Pregnancy 177 stress support internal homeostasis in two on glucagon, growth hormone, and cortisol ways. First, release of catecholamines by pe- response to moderate or intense exertion ripheral nerves serves to increase and redi- has not been examined. rect cardiac output to exercising muscle while maintaining \"adequate\" perfusion to Consequently, the nature and degree of nonexercising vascular beds. Second, the pregnancy-induced alterations of acute hor- medullary release of catecholamines, and monal response to exertion are largely the release of glucagon, cortisol, and growth unexamined. Possible direct or indirect ef- hormone result in providing the peripheral fects of these changes on fetal homeostasis circulation with fuel to maintain both in- during maternal exertion are likewise un- tense and sustained exertion. known. Little has been published about altera- MATERNAL tions in the hormonal response to exertion THERMOREGULATION DURING induced by pregnancy. Resting plasma nor- EXERCISE epinephrine and epinephrine levels are un- changed in pregnancy, though standing is Published studies of maternal thermoreg- associated with a reduced rise in norepi- ulation have examined gravidae only,during nephrine concentration in pregnancy.43 Ex- submaximal exertion lasting 20 to 30 min- ertion appears to produce a similar norepi- utes in a controlled laboratory environment nephrine response in pregnancy as in the of 19 to 21 °Cwith a relative humidityof 30% nonpregnant state.44,45 Insulin concentration to 55%. Two studies examined stationary does not appear to fall during mild exertion cycle exercise at approximately 60% during pregnancy46 but has not been exam- Vo2max,47,48 and one49 had subjects perform ined at more vigorous exercise. Glucagon, treadmill exercise at a maternal heart rateof which is increased in pregnancy, has been approximately 158 beats per minute (bpm) observed to rise twofold with materal exer- (approximately 60% Vo2max). Under these tion to a pulse of only 104,46 but this was not conditions, the range of mean rectal temper- confirmed in later studies.44 In the nonpreg- ature rise was 0.3 to 0.8°C during exercise, nant state, increased glucagon concentra- inversely related to gestational age (Fig. 10- tions are observed after only intense or pro- 1). Pregnant women appear to maintain longed exertion.29 The effect of pregnancy Figure 10-1. Resting and maximal rectal temperatures (at the bottom and top of each column, re- spectively) during,and 10 minutes after, a 20-minute cycle exercise period at 61%-64%maximal ox- ygen uptake. (Adapted from Clapp48).
178 Developmental Phases their core temperature within narrow limits, Early studies in human pregnancy exam- though maternal thermoregulatory capacity ined fetal heart-rate response to maternal during exertion under more stressful ambi- exertion using the same Doppler fetal mon- ent conditions has not been examined. As- itors used clinically on quiet, recumbent sociated fetal effects also have not been ex- women during labor. These reports de- amined. scribed frequent fetal bradycardia with only brief and mild maternal exertion,57,58 but the ACUTE EFFECTS OF MATERAL findings may have been confounded by mo- EXERTION ON THE FETUS tion artifact during maternal activity. Splanchnic perfusion falls linearly with Subsequent investigation has employed the percentage of Vo2max, as blood flow is two-dimensional sonographic fetal heart- redistributed to exercising muscle. A similar rate documentation. In one such study, 85 reduction in uterine blood flow with mod- submaximal and 79 maximal exercise erate and extreme maternal exertion during bouts59 produced no unexplained fetal bra- pregnancy has been demonstrated in dycardia (< 110 bpm) duringexertion. How- sheep50-52 and goats53 and suggested in hu- ever, postexertional fetal bradycardia was mans (Fig. 10-2).54-56 In sheep, this exer- noted within 3 minutes of cessation of max- cise-induced reduction of uterine perfusion imal aerobic effort in 19% (15 out of 79) of was found to be associated with a fall in fetal cases (Fig. 10-3). This bradycardia was not Po2 of 11% with moderate maternal exertion, associated with the duration of maximal aer- and 30% with exhausting exertion.51 How- obic exertion, changes in maternal blood ever, no measurable net lactate production pressure during and after exertion, or with by the conceptus has been observed under gestational age. It was more likely to occur these conditions. This suggests that oxygen in women with higher Vo2max values, sug- delivery is, in most fetal tissues, adequate gesting that maternal cardiovascular fitness for aerobic metabolism during these short- does not protect against this event. All fe- term experiments. tuses had normal fetal heart-rate patterns and fetal activity within 30 minutes of mater- Figure 10-2. Relationship between heart rate and uter- nal exercise, and the birth outcome in the ine blood flow as percent of control in near-terra preg- pregnancies with fetal bradycardia was un- nant sheep: o = rest, a = 10-minute exercise at70% complicated. V40o-2mmianxu; t•e = 10-minute exercise at 1(F00ro%mVLo2omtgaexr;inAg,=51 exercise at 70% Vo2max. These data suggest that fetal homeostatic with permission). reserve is not compromised by even ex- treme levels of maternal exertion in the human. The possible adverse impact of ma- ternal upright posture on fetal homeostasis during maternal recovery remains to be ex- plored. The observed postexertional fall in stroke volume in exercising gravid women may indicate that visceral perfusion may be compromised in pregnancy under these conditions. Observations of baseline fetal heart rate before, during, and after maternal exertion has generally shown a 10to 15bpm increase in fetal heart rate with moderate exertion lasting 30 minutesor more. Generally mater- nal exertion at 60%Vo2max which lasts less than 20 minutes will not produce fetal tachy- cardia. Exertion at this level which lasts 20
Pregnancy 179 to 30 minutes will produce a rise in fetal heart rate which correlates with gestational age over 20to 36weeks. This response does not correlate with the minor changes in ma- ternal core temperature (0.3°C) observed in these subjects, however.47 MATERNAL EXERCISE TRAINING EFFECTS ON FETAL GROWTH AND PERINATAL OUTCOME The epidemiology of the workplace envi- ronment and activity and maternal and peri- natal outcome occupies a large body of lit- erature. Discussion here will be limited to studies examining the association of recre- ational exercise with maternal and perinatal outcome. Prospective studies of recrea- tional exertion can be divided into nonran- domized and randomized, controlled com- parisons of exercising and sedentary pregnant women. Nonrandomized studies have shown both no effect on maternal weight gain60 and significantly reduced ma- teral weight gain caused by chronic mater- nal exercise.61 Likewise, nonrandomized ob- servations have documented either no effect of chronic maternal exercise on birthweight and duration of pregnancy60,62 or a significant reduction in birth weight, percentile birth weight, percentage body fat,63 and earlier gestational age at birth.61,64 Exercisingmoth- ers were found to have either a lower rate of labor complications60,64 or no significant dif- ference from their nonrandomized con- trols.62 It should be noted that most of these nonrandomized studies63-65 examine the ef- fect of the cessation of maternal recreational exertion before or early in pregnancyamong women who are exercise enthusiasts. The remainder are simply comparisons of Figure 10-3.Fetal heart rate following maximal exer- onds during the postexercise period, using videotaped tion during 14episodes of fetal bradycardia. Fetal heart recordings of two-dimensional fetal imaging. Predece- rate was averaged over 10 cardiac cycles every 30 sec- leration baseline fetal heart rate and nadir fetal heart rate are noted for each deceleration. Zero time is time of cessation of maximal effort. (From Carpenter,59 with permission).
180 DevelopmentalPhases women who have self-selected exercise pro- Available data suggest that maternal exer- grams or sedentary activity. tion does not predispose to preterm labor. Two randomized, controlled trials66,67 ex- RECOMMENDATIONS ABOUT amined the effect of instituting exercise RECREATIONAL EXERCISE training during pregnancy in sedentary pregnant women. Only one provided ob- The limited scope of applied research re- served exercise training in a laboratory en- garding the effects of pregnancy on acute ex- vironment.67 Both studies documented ob- ercise and training and the effects of exer- jective signs of cardiovascular training effect tion on pregnancy limit the advice that can in the groups randomized to exercise train- be confidently given to the pregnant patient. ing; however, in contrast to the nonrandom- In 1985, the American College of Obstetri- ized investigations, neither randomizedtrial cians and Gynecologists published two pre- showed any effect of maternal exercise scriptive articles,70,71 which commented on training on maternal weight gain, length of exercise during pregnancy. These recom- gestation, birth weight, Apgar scores, or mendations preceded much of the clinical mode of delivery. One study66 suggested that research performed in this area. As such, primigravid trainers had a shorter second they were an attempt to form a consensus stage of labor. opinion about principles of maternal and fetal safety during maternal exertion, and Differences between the results of non- they reflected a necessarily conservative ap- randomized and randomized prospective proach to exercise in pregnancy that could studies suggest that self-selected women be used, practically, in a clinical setting. may differ in daily activity, percentage body Some later studies have addressed some of fat, caloric intake or food type, or other fac- these issues. tors that affect fetal growth, medical treat- ment during labor, and maternal and peri- The principles documented in these pub- natal outcome. Some of the nonrandomized lished guidelines are listed below. In italics, studies are detraining studies rather than the uncertainty attending these guidelines investigations of training effects in seden- or modifying data available from subse- tary women, and thereby present problems quently published research are discussed. in applying findings in atheletes to the more common, inactive pregnant woman. Women 1 Maternal joints become more unstable who enter pregnancy with a history of fre- during pregnancy and may be more quent vigorous exertion may differ metabol- prone to injury during exertion. Exer- ically from those who are relatively seden- cises should avoid \"ballistic\" move- tary. ment and extreme extension and flexion of joints. No observationalor experimen- Transabdominal pressure transducer tal studies have quantified the risk of joint monitoring of pregnant women during ex- injury during pregnancy. These proscrip- ercise has shown, in one study,68that uterine tions may reduce injury, however. contractions are associated withnonrecum- bent types of exercise. Another investiga- 2 More physically fit individuals will per- tion,69 however, examined uterine contrac- form a given task at a relatively lower tions by the same method immediately after percentage of maximal aerobic capac- the cessation of maternal exertion and ity. It is therefore desirable for women found no increased uterine activity. These to become aerobically trained before studies and practical experience in the use pregnancy and thereby reduce fetal risk of these transducers in laboring women sug- of asphyxia and bradycardia duringma- gest that the uterine activity detected in up ternal exertion during pregnancy. Di- to 50% of gravidae during exercise is likely to represent artifact due to maternal motion.
Pregnancy 181 rect observation of fetal heart-rate re- carbohydrates during exertion if exercise sponse during maternal exertion has is carried out at a higher percentage of shown no fetal heart rate decelerations aerobic capacity, so it may be desirable during exertion of any relative intensity, during pregnancy to exercise at levels that and none following maternal exertion up elicit maternal heart rates of less than 150 to a maternal pulse of 150 bpm in the ma- bpm. ternal age range of 21 to 37 years of age. 5 Exercise during pregnancy may result The occasional fetal bradycardia that fol- in premature labor due to release lows maximal maternal exertion is more of norepinephrine. Experimental data common in the more aerobically fit show no consistent evidence of increased mother. Maternal exertion may increase uterine contractions immediately follow- the baseline fetal heart rate.72 However, ing exertion. Preterm labor among exer- exercise-associated fetal tachycardia and cisers does not appear to be increased in episodic bradycardia are unassociated either detraining or training studies. with any measurable fetal or neonatal 6 Previously sedentary women should morbidity.59 The usually recommended engage in activity of very low intensity warm-up and slow cool-down periods and avoid exertional intensity known to with exercise should probably be used increase exertional cardiovascular fit- during pregnancy. ness. Limited human experimental data 3 Pregnant women may develop a high show no increased maternal or fetal com- maternal core temperature during ex- promise during and after acute exertion. ercise exceeding 15 minutes, especially Pregnant women with lower Vo2max val- in hot and humid environments. High ues had a lower rate of fetal bradycardia maternal core temperature may be as- after maximal exertion,59 suggesting that sociated with teratogenesis or respira- prior sedentary lifestyle is not a contrain- tory compromise in animals, suggesting dication to vigorous exertion during preg- risk in the exercising mother. Human nancy. experiments describe only a 0.3 to 0.8°C 7 Pregnant women should practice good rise in maternal core temperature with nutritional principles (see below) and moderate to severe maternal exertion of avoid cigarettes and alcohol. The vaso- 30 minutes' duration,47,48,73 an increase of dilatory effects of alcohol and vasocon- little physiologic consequence. The effect strictive and hypoxemic effects of ciga- of maternal exertion under conditions of rette smoking may compromise the high ambient temperature and humidity homeostatic reserve of the mother and the on fetal homeostasis and core tempera- fetoplacental unit during maternal exer- ture has not been examined. tion. Women who smoke and drink during 4 Maternal fasting glucose levels are sig- pregnancy should probably avoid exer- nificantly lower than in the nonpreg- tion at times when exposed to these drugs. nant state. Since pregnant women use No human observational studies or exper- more carbohydrate during exertion, hy- iments have been performed examining poglycemia may occur during exertion. these interactions directly. Little human experimental evidence is 8 Women whose pregnancies are com- available about maternal glycemic re- promised by any maternal diseases or sponse to exertion. Animal experiments any untoward symptoms should con- performed in the nonpregnant state indi- tact their physician for consultation. cate that both sympathetic and glucagon The importance of consultation of a response to exertion must be ablated to patient with her physician should be em- cause exertional hypoglycemia. Gravidae phasized. Though data are not available, consume a relatively higher proportion of caution regarding exertion in many con-
182 Developmental Phases ditions complicating pregnancy should be affected by maternal exercise. Thesig- counseled byphysicians. nificance of these interactions is impos- We use several principles when counsel- sible to estimate; thus, we remaincau- ing pregnant women regarding exercise: tious in our counseling of potentially 1 We recognize the value of continued affected pregnant patients. recreation during pregnancy, which for 6 Patients with a history of poor preg- many women includes vigorous exer- nancy outcome due to repeated abor- tion. Unless prior observational or ex- tion, abruptio placenta, preterm labor, perimental data or the individual cir- or preterm rupture of membranes are cumstances of the patient's pregnancy probably not compromised by exercise appear to contradict a proposed exer- in pregnancy, based on limited studies cise activity during pregnancy, we do in normal women. Appropriate investi- not proscribe exertion for the patient. gation of exercise effects on patients 2 Relative exertional intensity, as de- with these histories have not been per- scribed in terms of percentage of formed, however. We counsel patients Vo2max, produces similar cardiovascu- with such histories who desire to exer- lar, respiratory, and hormonal re- cise about our lack of knowledge, and sponses. Likewise, fetal homeostasis is about their potential sense of responsi- similarly maintained at a given relative bility should another mishap occur in exertional intensity, regardless of the the present pregnancy. In this circum- exertional fitness of the experimental stance, however, we are nondirective in animal. We infer that this is also true for our counseling. Patients with histories pregnant patients and allow physical of incompetent cervix, DES exposure, or exertion in all healthy patients up to a with uterocervical abnormalities are heart rate of 150 bpm. Since heart rate counseled to avoid exertion during is difficult to monitor during competi- pregnancy. tive sports and levels of peak exertion tend to be high, we discourage compet- NUTRITIONAL REQUIREMENTS itive exertion for pregnant women. OF PREGNANT EXERCISERS 3 Exercise studies during pregnancy have been limited to short bouts of exertion It seems appropriate to advise pregnant under \"comfortable\" ambient condi- exercisers also about possible changes in tions. Since exertion for prolonged pe- nutritional requirements to support the en- riods or with high heat and humidity ergy demands of exercise and the increased has not been examined in human preg- caloric costs of accretion of maternal and nancy, we discourage exercise under fetal tissues. Pregnancy, but not exercise, these conditions in pregnant patients. substantially increases dietary protein re- 4 Pregnant patients are probably more quirements. Other than fetal demands for prone to trauma because of changes essential free fatty acids, neither exercise in weight distribution and resulting nor pregnancy requires a net increase in di- \"clumsiness.\" Consequently, we cau- etary fat. tion patients about potentially trau- matic sports, especially in the last half Estimates of increased caloric needs of of pregnancy, when the uterus is more pregnancy were originally based on cross- exposed to frontal trauma. sectional data of increased maternal and 5 Fetal homeostasis during pregnancy fetal mass in pregnancy.73,74The fetal mass of compromised by uteroplacental insuf- 3.5 kg, the placental mass of 0.6 kg, the in- ficiency, cardiac or respiratory disease, crease in uterine and breast mass of 5 kg,of or significant anemia may be adversely maternal fat of 4 kg, and the estimated in- crease in metabolic rate were used to esti-
Pregnancy 183 mate the total caloric cost of pregnancy to amounts will be provided by a balanced diet be approximately 83,000 kcal. This estimate with sufficient increased calories. The exer- suggests that an increase of ~250 kcal in cise-related requirements for thiamine, nia- daily caloric intake is needed in pregnancy, cin, riboflavin, and pantothenic acid like- consistent with the FAO/WHO/UNU,75 the wise are probably supported by a calorically United Kingdom Department of Health and adequate diet. Social Security,76 and the National Research Council.77 Longitudinal investigations of Mineral needs, in the form of iron and cal- pregnancy begun prior to conception pro- cium, are probably not increased in exercis- vide different data, however. A cohort of 162 ing individuals. Pregnancy results in a fetal women from Scotland and the Netherlands accretion of 300 mg of elemental iron and a underwent prospective measurements of maternal erythropoietic requirement of 500 weight, body fat, dietary intake, metabolic mg. Exercise training will produce an in- rate at rest, and daily activity pattern.78 The crease in plasma volume and erythrocyte estimated increased energy cost of preg- mass which requires a transient increase in nancy was ~69,000 kcal. The increase in iron utilization. Recommendations for the dietary intake during pregnancy was esti- daily intake of iron (30 to 60 mg of elemental mated based on fairly rigorous weighed-in- iron) and calcium (1200 to 1500 mg of ele- ventory 5-day measurements performed mental calcium) duringpregnancy will meet every 2 to 4 weeks during pregnancy. These the needs of exercising as well as sedentary estimates suggested that the average incre- pregnant women. ment in dietary intake duringpregnancy was only ~22,000 kcal. The 47,000-kcal discrep- SUMMARY ancy suggests either that the estimates ofca- loric intake are in error or that there is a re- Both pregnancy and exercise produce duction in physical activity and an increase profound adaptive cardiovascular and en- in mechanical efficiency during pregnancy. docrine responses which affect fetal homeo- Nevertheless, during normal pregnancy stasis. The early cardiovascular and hema- with documented sedentary lifestyle, daily tologic changes of pregnancy include incremental caloric intake appears to be 80 increased stroke volume, increased cardiac to 100 kcal/d in the first half of pregnancy, output, decreased peripheral vascular re- and approximately 150 to 200 kcal/d during sistance, increased venous compliance, in- the second half. Since chronic exercise may creased minute respiration, and increased increase basal metabolic rate and the char- plasma and red cell volume. These \"adap- acter, duration, frequency, and intensity of tations\" occur well before the fetoplacental exercise will otherwise affect the increased unit develops the increased gas and nutrient caloric cost of exertion, these estimates are transport that is supported by these complex and need to be individualized. changes. Since maternal weight gain probably offers a reproducible correlate with fetal growth in Exercise in pregnancy is associated with the second half of uncomplicated, sedentary many of the same physiologic responses as- pregnancy, weekly weight gain may provide sociated with exertion in the nonpregnant a practical measure of the adequacy of ca- state. Vasoconstriction occurs in vascular loric support in exercising women. The util- beds, except those serving exercising mus- ity of maternal weight gain as a measure of cle. Mild exertion induces increases in pulse fetal nutritional adequacy in pregnancy in and stroke volume,which both contribute to exercising women has not been adequately increased cardiac output. Limited data sug- tested, however. gest that the neuroendocrine response and insulin and glucagon response to exertion Requirements for most vitamins are in- during pregnancy are similar to those found creased during pregnancy, but adequate in the nonpregnant state. However, preg-
184 Developmental Phases nancy is associated with a decreased arte- training by athletes after conception may re- riovenous O2 difference and an increased duce fetal birth weight, though this thesis stroke volume, which may impact on re- requires further investigation. sponse to intense physical exertion. For ex- ample, during cycle exercise, increases in Clinical recommendations for patients de- stroke volume appear to contribute to incre- sirous of engaging in recreational exercise mental cardiac output at extreme exertional are limited by the small number of clinical intensity, which does not occur in nonpreg- studies available. Consequently, current nant humans. published recommendations are conserva- tive, recognizing that the benefits of mater- The increased weight in pregnancy and nal recreational exercise for the fetus are the increase in metabolically active fetopla- probably miminal and the potential risks un- cental tissue results in higher pulse, cardiac known. output, and oxygen uptake at rest and at sim- ilar external workloads during pregnancy, REFERENCES compared to postpartum values. Similar ex- ternal exertional power thereby requires ex- 1. Hytten FE, and Paintin DB: Increase in ertion at a higher percentage of Vo2max dur- plasma volume during normal pregnancy. J ing pregnancy. Pregnancy does not affect Obstet Gynaecol Br Com 70:402, 1963. the weight-specific oxygen uptake at rest and duringweight-supported exertion, how- 2. Lund CJ, and Donovan JC: Blood volume dur- ever. ing pregnancy. Am J Obstet Gynecol 98:393, 1967. Maternal thermoregulation maintains the core maternal temperature within 0.3 to 3. Phippard AF, Horvath JS, Glynn EM,et al: Cir- 0.8°C in human pregnancy, when exercise is culatory adaptation to pregnancy—serial limited to 20 to 30 minutes. The effect of studies of haemodynamics, blood volume, more prolonged exertion under conditions renin and aldosterone in the baboon. J Hy- of high ambient heat or humidity have not pertens 4:773,1986. been examined. 4. Longo LD: Maternal blood volume and car- Fetal response to maternal exertion has diac output during pregnancy: a hypothesis been examined most directly in the ungulate of endocrinologic control. Am J Physiol model. Uterine perfusion falls in proportion 245:R720,1983. to duration and intensity of maternal exer- tion, but even under conditions of extreme 5. Capeless EL, and Clapp JF: Cardiovascular exertion, fetoplacental oxygen uptake is changes in early phase of pregnancy. Am J maintained. Human studies using two-di- Obstet Gynecol 161:1449, 1989. mensional fetal imaginghave shown no fetal heart-rate decelerations during even maxi- 6. Laird-Meeter K, van de Ley G, Bom TH, et al: mal maternal exertion, nor following sub- Cardiocirculatory adjustments during preg- maximal maternal exercise. Frequent fetal nancy—an echocardiographic study. Clin heart-rate decelerations observed following Cardiol 2:328,1979. maximal maternal exertion suggest that fe- toplacental perfusion or blood pressure may 7. Rubier S, Damani PM, and Pinto ER:Cardiac be disturbed by this maneuver. size and performance during pregnancy es- timated with echocardiography. Am JCardiol Studies of maternal and perinatal out- 40:534,1977. come following chronic maternal exercise are largely flawed by nonrandom assign- 8. Knuttgen HG, and Emerson K: Physiological ment of subjects to comparison groups. The response to pregnancy at rest and during ex- few randomized trials suggest that exercise ercise. J Appl Physiol 36:549, 1974. training can be instituted during pregnancy without morbid effect. Continued exercise 9. Pernoll ML,et al: Oxygen consumption at rest and during exercise in pregnancy. Respir Physiol 25:285, 1975. 10. Sady SA, et al: Cardiovascular response to cycle exercise during and after pregnancy. J Appl Physiol 65:336, 1989. 11. Ueland K, et al: Maternal cardiovascular dy- namics. Am J Obstet Gynecol 104:856,1969. 12. Fawer R, et al: Effect of the menstrual cycle, oral contraception and pregnancy on fore- arm blood flow, venous distensibility and
Pregnancy 185 clotting factors. Eur J Clin Pharmacol 13:251, gon and plasma catecholamine responses to 1978. graded and prolonged exercise in man. J 13. Barwin BN, and Roddie 1C: Venous distensi- Appl Physiol 38:70, 1975. bility during pregnancy determined by 30. Christensen NJ, et al: Catecholamines and ex- graded venous congestion. Am J Obstet Gy- ercise. Diabetes 28(Suppl 1):58,1979. necol 125:921,1976. 31. Scheurink AJW, et al: Adrenal and sympa- 14. Boutourline-Young H, and Boutourline- thetic catecholamines in exercising rates. J Young E: Alveolar carbon dioxide levels in Appl Physiol 66:R155,1989. pregnant parturient and lactating subjects. J 32. Pruett EDR: Plasma insulin during prolonged Obstet Gynaecol Br Com 63:509,1956. work at near maximal oxygen uptake. J Appl 15. Clapp JF: Cardiac output and uterine blood Physiol 29:155, 1970. flow in the pregnant ewe. Am J Obstet Gyne- 33. MikinesKJ, Sonne B, and Farrell PA: Effect of col 130:419,1978. physical exercise on sensitivity and respon- 16. Carpenter MW, et al: Effect of maternal weight siveness to insulin in humans. Am J Physiol gain during pregnancy on exercise perfor- 254:E248,1988. mance. J Appl Physiol 68:1173, 1990. 34. Bottger I, et al: The effect of exercise on glu- 17. Rowell LB: Circulatory adjustments to dy- cagon secretion. J Clin Endocrinol Metab namic exercise. In Rowell (ed): HumanCir- 35:117,1972. culation. Regulation during Physical Stress. 35. VanHelder WP, Casey K, and Radomski MW: Oxford University Press, New York, 1986, p Regulation of growth hormone during exer- 226. cise by oxygen demand and availability. Eur 18. Karpman VL: Cardiovascular System in Phys- J Appl Physiol 56:628, 1987. ical Exercise. CRC Press, Boca Raton, FL, p 36. Ueland K, Novy MJ, and Metcalfe J: Cardio- 140. respiratory responses to pregnancy and ex- 19. Christensen NJ, and Galbo H: Sympathetic ercise in normal women and patients with nervous activity during exercise. Annu Rev heart disease. Am J Obstet Gynecol 115:4, Physiol 45:139, 1983. 1973. 20. Dempsey JA: Is the lung built for exercise? 37. Lehmann V, and Regnat K: Untersuchung sur Med Sci Sports Exerc 18:143,1986. korperlichen belastungsfahigkeit schwan- 21. Brooks GA, and Fahey TD: Metabolic re- geren frauen. Der einfluss standardisierter sponse to exercise In Brooks GA, and Fahey arbeit auf herzkreislaufsystem, ventilation, TD (eds): Exercise Physiology: Human Bio- gasaustausch, kohlenhydratstoffwechsel und energetics and its Applications. John Wiley & saure-basen-haushalt. Z Beburtshilfe Peri- Sons, New York, 1985, p 189. nato 180:279, 1976. 22. Jones NL, and Ehrsam, RE: The anaerobic 38. Blackburn MW,and Calloway DH: Heart rate threshold. Exerc Sport Sci Rev 10:49,1982. and energy expenditure of pregnancy and 23. McArdle WD, Katch FI, and Katch VL: Exer- lactating women. Am J Clin Nutr 42:1161, cise Physiology, Energy, Nutrition, and 1985. Human Performance. Lea & Febiger, Phila- 39. Sady SA, et al: Prediction of VO2max during delphia, 1986. cycle exercise in pregnant women. J Appl 24. Astrand PO, and Rodahl K: Physical perfor- Physiol 65:657, 1988. mance. In Astrand PO, and Rodahl K (eds): 40. Morton MJ, et al: Exercise dynamics in late Textbook of Work Physiology. Physiological gestation: Effects of physical training. Am J Bases of Exercise. New York, 1986, p 295. Obstet Gynecol 152:91,1985. 25. Fredholm B: Inhibition of fatty acid release 41. Ryan ED, O'Sullivan MJ, and Skyler JS: Insu- from adipose tissue by high arterial lactate lin action during pregnancy: Studies with concentrations. Acta Physiol Scand (Suppl the euglycemic clamp technique. Diabetes 330):77, abstract #106,1969. 34:380, 1985. 26. Felig P, and Wahren J: Role of insulinand glu- 42. Hjollund E, et al: Impaired insulin receptor cagon in the regulation of hepatic glucose binding and postbinding defects of adipo- production during exercise. Diabetes 28 cytes from normal and diabetic pregnant (Suppl 1):7175,1979. women. Diabetes 35:598, 1986. 27. Horton ES: Exercise and diabetes mellitus. 43. Barren WM, et al: Plasma catecholamine re- Med Clin North Am 72:1301, 1988. sponses to physiologic stimuli in normal 28. Hoelzer DR, et al: Glucoregulation during ex- human pregnancy. Am J Obstet Gynecol ercise: Hypoglycemia is prevented by redun- 154:80, 1986. dant glucoregulatory systems, sympatho- 44. Artal R. Wiswell R, and Romeo Y:Hormonal chromaffin activation and changes in islet responses to exercise in diabetic and nondi- hormone secretion. J Clin Invest 77:212,1986. abetic pregnant patients. Diabetes 34(Suppl 29. Galbo H, Hoist J, and Christensen NJ:Gluca- 2):7880, 1985.
186 Developmental Phases 45. Airaksinen KEJ, et al: Effect of pregnancy on cise and pregnancy outcome. Med Sci Sports autonomic nervous function and heart rate in Exerc 16:556, 1984. diabetic and nondiabetic women. Diabetes 62. Hall DC, and Kaufmann DA: Effects of aerobic Care 10:748,1987. and strength conditioning on pregnancy out- comes. Am J Obstet Gynecol 157:1199, 1987. 46. Artal R, et al: Exercise in pregnancy I. Mater- 63. Clapp JF, and Capeless EL: Neonatal morpho- nal cardiovascular and metabolic responses metrics after endurance exercise during in normal pregnancy. Am J Obstet Gynecol pregnancy. Am J Obstet Gynecol 163:1805, 140:123,1981. 1990. 64. Clapp JF: The course of labor after endurance 47. Carpenter MW, et al: Maternal exercise du- exercise during pregnancy. Am J Obstet Gy- ration and intensity affect fetal heart rate. necol 163:1799, 1990. 1989 American College of Sports Medicine 65. Clapp JF: The effects of maternal exercise on Annual Meeting. early pregnancy outcome. Am J Obstet Gy- necol 161:1453, 1989. 48. Clapp JF: The changing thermal response to 66. Kulpa PJ, White BM, and Visscher R:Aerobic endurance exercise during pregnancy. Am J exercise in pregnancy. Am J Obstet Gynecol Obstet Gynecol 165:1684, 1991. 156:1395,1987. 67. Carr SR, et al: Obstetrical outcome in aerobi- 49. Jones RL, et al: Thermoregulation during aer- cally trained women. Am J Obstet Gynecol obic exercise in pregnancy. Obstet Gynecol SPO Abstracts 166:l(pt 2):380 (abstr 376), 65:340, 1985. 1992. 68. Durak EP, Jovanovic-Peterson L, and Peter- 50. Clapp JF: Acute exercise stress in the preg- son CM: Comparative evaluation of uterine nant ewe. Am J Obstet Gynecol 136:489,1980. response to exercise on five aerobic ma- chines. Am J Obstet Gynecol 162:754, 1990. 51. Lotgering FK, Gilbert RD, and Longo LD: Ex- 69. Veille JC, et al: The effect of exercise on uter- ercise responses in pregnant sheep: Blood ine activity in the last eight weeks of preg- gases, temperatures and fetal cardiovascular nancy. Am J Obstet Gynecol 151:727, 1985. system. J Appl Physiol 55:842,1983. 70. ACOG Technical Bulletin: Women and Exer- cise. ACOG Technical Bulletin Number 87, 52. Chandler KD, and Bell AW: Effects of mater- September, Washington DC, 1985. nal exercise on fetal and maternal respiration 71. ACOG Home Exercise Programs: Exercise and nutrient metabolism in the pregnant ewe. during pregnancy and the postnatal period. JDev Physiol 3:161, 1981. May, Washington DC, 1985. 72. Collings C, and Curet LB: Fetal heart rate re- 53. HohimerAR, et al: Maternal exercise reduced sponse to maternal exercise. Am J Obstet Gy- myoendometrial blood flow in the pregnant necol 151:498, 1985. goat. Fed Proc 41:1490, 1982. 73. Hytten FE, and Leitch I: The Physiology of Human Pregnancy, ed 2. Blackwell, Oxford, 54. Morris N, Osborn SB, and Payling Wright H: 1971. Effect on uterine blood-flow during exercise 74. Hytten FE, and Chamberlain GVP: Clinical in normal and pre-eclamptic pregnancies. Physiology in Obstetrics. Blackwell, Oxford, Lancet 2:481, 1956. 1980. 75. FAO/WHO/UNU: Energyand protein require- 55. Morrow RJ, Knox Ritchie JW, and Bull SB: ments. WHO Tech Rep Ser No 724. World Fetal and maternal hemodynamic responses Health Organization,Geneva, 1985. to exercise in pregnancy assessed by Dopp- 76. Department of Health and Social Security: ler ultrasonography. Am J Obstet Gynecol Recommended daily amounts of food energy 160:138, 1989. and nutrients for groups of people in the United Kingdom. Rep Health Soc Subj 15, 56. Rauramo I, and Forss M: Effect of exercise on 1979. placental blood flow in pregnancies compli- 77. National Research Council, Food and Nutri- cated by hypertension, diabetes or intrahe- tion Board: Recommended dietary allow- patic cholestasis. Acta Obstet Gynecol Scand ances. National Academy, Washington DC, 67:15, 1988. 1989. 78. Durnin JV: Energy requirements of preg- 57. Artal R, Paul RH, Romeo Y, and Wiswell R: nancy. Diabetes 40(Suppl 2):152, 1991. Fetal bradycardia induced by maternal exer- cise. Lancet 2:258, 1984. 58. Jovanovic L, Kessler A, and Peterson CM: Human maternal and fetal response to graded exercise. J Appl Physiol 58:1719, 1985. 59. Carpenter MW, et al: Fetal heart rate re- sponse to maternal exertion. JAMA 259:3006, 1988. 60. Dale E, Mullinax KM, and Bryan DH: Exercise during pregnancy: Effects on the fetus. Can J Appl Sport Sci 7:98, 1982. 61. Clapp JF, and Dickstein S: Endurance exer-
11CHAPTER Menopause* MORRIS NOTELOV1TZ, M.D., Ph.D., and MONA M. SHANGOLD, M.D. MENOPAUSE IN PERSPECTIVE MUSCLE TISSUE AND STRENGTH Age-Related Loss of Muscle Tissue OSTEOPOROSIS AND BONE HEALTH and Strength Strength Training Osteogenesis: A Brief Overview Exercise and Osteogenesis: Clinical OTHER MENOPAUSAL PROBLEMS: VASOMOTOR SYMPTOMS Research OTHER AGE-RELATED CHANGES ATHEROGENIC DISEASE AND Exercise and Adipose Tissue CARDIORESPIRATORY FITNESS Exercise and Osteoarthrosis Lipids, Lipoproteins, and Exercise EXERCISE AND WELL-BEING Aerobic Power MENOPAUSE IN PERSPECTIVE Menopause is a natural phenomenon that usually lasts about 1week—thedura- tion of the last menstrual period. It is the biologic marker of the gradual but per- sistent decrease in ovarian steroidogenesis that precedes the cessation of men- struation by about 15years and that postdates that event by a similar duration. This period of reproductive senescence is known as the climacteric. The differ- entiation between \"menopause\" and the \"climacteric\" involves more than semantics, since it serves to illustrate that the midlife physical and psychologic needs of women extend over a 30-year continuum.There are two additionalfea- tures of note: (1) the attenuation in endocrine function of the ovarian follicle affects many systems remote from the reproductive tract; and (2) the climacteric occurs at a time when certain age-related changes become apparent, so that one must differentiate between biologically induced and chronologically induced pathophysiology. *Supported by grants from the National Insti- this chapter, the period is more properly called tute on Aging R01 AG 00976, Nautilus Sports/ the \"climacteric,\" \"menopause\" is certainly the Medical Industries, Inc. more commonly used term. tAlthough, as discussed at the beginningof 187
188 Developmental Phases The date of menopause can be accurately terns. The late climacteric is often associ- pinpointed, but it is a retrospective diagno- ated with conditions resulting from chronic sis: a year of amenorrhea has to pass before estrogen deprivation—chronic atrophic the clinical diagnosis can be confirmed.The vaginitis, the urethral syndrome, and uri- mean age of onset of menopause in western nary incontinence. societies is 51 years.1 The climacteric may be empirically but pragmatically catego- Although the conditions just listed have rized into three decades of clinical presen- an impact on an individual's quality of life, tation and need (Fig. 11-1): the earlyclimac- none is life-threatening. There are, however, teric (age 35 to 45), premenopausal and two asymptomatic potential complications postmenopausal periods (age 46 to 55), and of the late climacteric that may have a seri- the late climacteric (56 to 65).2 Contrary to ous adverse effect and that are responsible the theory that follicular depletion is the for much of the morbidity and mortality as- cause of menopause, primordialfollicles are sociated with older age in women: osteopo- frequently found in the ovaries of postmeno- rosis and atherogenic disease. In the United pausal women, but they are unable to re- States, the total number of hip fractures spond to stimulation of the pituitary gonad- among white women was 158,000 in 1986, otropins—FSH and LH. The resultant and this number is expected to increase to alteration in ovarian function brings about 252,000 in the year 2020 and to 367,000 by the dysfunctionaluterine bleeding patterns the year 2040.3 Of this figure, approximately that characterize this phase. As the climac- 12% to 20% will die as a result of factors di- teric progresses, the decrease in estradiol rectly attributable to their hip fracture.4 production results in menopause and in a Only a third of the survivors will regain nor- number of so-called hormone-dependent mal activity.5 Of all hip fractures, 70%to 80% symptoms such as hot flushes and changes affect women. The total annual cost of hip in temperament, mood, and sleeping pat- fractures was approximately $7.2 billion in 1984, and this cost, adjusted for 5% inflation, Figure 11-1. Diagrammatic representation of the menopause as a single event in the larger context of the climacteric. (From Notelovitz2 with permission.)
Menopause 189 is expected to increase to $240 billion by issue is the fact that bone is a living tissue 2040.3 This cost, of course, does not take into and needs to be treated as such. account the physical and psychologic pain suffered by these women. Osteogenesls: A Brief Overview Bone formation depends upon a five-stage In 1989, approximately 500,000 persons died from ischemic heart disease, the lead- cycle that results in \"old\" bone being re- ing cause of death in the United States.6 An- moved and replaced with \"new\" bone. Nor- nual health-care costs for cardiovascular mally, this process is coupled; the amount of disease alone exceed $135 billion, while the old bone removed is replaced with an equal added costs of related injury and disability amount of freshly formed bone. Initiation of exceed $170billion.7 Cardiovascular disease the cycle is dependent upon the recruitment has a significant influence on thewell-being and activation of osteoclasts. This activity of the fastest-growing age group in the usually takes place on the inner aspect of the United States: an estimated 1000 individuals bone's surface—the endosteal layer—and join the ranks of the elderly every day.8 A results in the dissolution of bone mineral woman aged 65 can now expect to live an ad- and collagen, and the formation of a cavity. ditional 18.8 years (14.5 years for men).9 Resorption ceases when the mean depth of the cavity reaches 60 um (trabecular bone) Exercise can play an important role in en- and 100 urn (cortical bone) from the sur- suring an appropriate quality of life in mid- face.11 At this point, mononuclear cells lay dle age and later, but to be maximally effec- down a highly mineralized, collagen-poor tive, it needs to be introduced as a bone matrix known as cement substance. It premenopausal lifestyle—hence the em- is from this surface that new bone is laid phasis on recognizing the climacteric as an down by osteoblasts. These cells probably important transitional phase in the patho- originate from bone marrow stromal cells genesis of potentially preventable disease. (preosteoblasts), thereby sharing the abil- ity of another cell type, the fibroblasts, to OSTEOPOROSIS AND BONE synthesize collagen.11 The stimulus for os- HEALTH teoblast recruitment may be mechanical owing to humoral and/or locally produced Osteoporosis is preventable. It is a con- substances (for example, human skeletal dition that is relatively uncommon in men growth and other bone growth factors).12 and in black women, owing in part to their having a greater bone mass. Cohn and co- The osteoblasts are responsible for the workers10 examined the skeletal and muscle synthesis of collagen, which is the main mass of normal black women and found that component of newly formed bone matrix, or their total body calcium was 16.7% higher osteoid. The latter matures and is latermin- than that of age-matched white women. eralized by a process that largely depends More than half of this difference (9.7%) was on an adequate supply of calcium and phos- calculated to be due to a greater muscle phate and the formation of hydroxyapatite mass in the black women. Thus, despite the crystals.10 At a microstructural level, numer- complexity of bone physiology, two practi- ous small crystallites of hydroxyapatite may cal issues need to be addressed: (1) women' be seen in intimate juxtaposition and in need to acquire as much bone as possible highly organized geometric arrangements before menopause, and (2) the rate at which with collagenfibrils.11 bone is lost thereafter needs to be modu- lated. Exercise plays a pivotal role, in that it The elastic and tensile strength of bone is one of the few knownmeans of stimulating depends in large measure on this interrela- new bone formation. Central to the entire tionship. Another very important determi- nant of the mechanical strength of bone is the orientation of the collagen fibrils in the
190 Developmental Phases bone matrix and the three-dimensional net- rangement of vertical and horizontaltrabec- work of plates and bars found especially in ulae (Fig. 11-2). Interruptionof this support trabecular bone (such as vertebrae), and to system—for example, loss of horizontal tra- a lesser extent in cortical bone (forexample, beculae as a result of aging—can impair the the radius), resulting in a scaffoldlike ar- structural integrityof the bone and result in Figure 11-2. Scanning electron micrograph of an iliac crest biopsy from (A) a normal subject auu (fi) a woman with osteoporosis. Contrast the normal contiguous vertical and horizontal trabeculae with the thinning decreased number and loss of continuity of the trabecular plates in osteoporosis. (From Dempster DW, et al: A simple method for correlative light and scanning electron microscopy of human iliac crest bone biopsies: Qualitative observations in normal and osteoporotic subjects. J Bone Min Res 1(1):15, 1986, with permission.)
Menopause 191 fracture, even in the presence of a relatively 30 years from age 50 to age 80.13 Trabecular normal amount of bone mineral.13 This is an bone accrual reaches its maximum during important consideration when prescribing the mid to late 20s and is followed thereafter exercise for older women. by a linear loss of bone.15 Others maintain that the trabecular bone loss pattern equals Types and Rates of Bone Loss that of cortical bone, with a loss of at least 0.19% per year before menopause and at As mentioned above, there are two types least 1.1% thereafter. Thus an estimated of bone: cortical and trabecular. Cortical 31.7% of trabecular bone is lost during the (compact) bone is found primarily in the ap- 50-year span between 30 and 80 years of pendicular skeleton (for example, in the age.13 The greater the bone mineralcontent femur, tibia, and fibula of the lower limbs, at bone mass maturity (maximum), of and in the humerus, ulna, and radius of the course, the more an individual can afford to arms). Cortical bone constitutes 80% of the lose, so there is a need to focus on the ac- total skeleton but is metabolically less ac- crual of bone during youth rather than on tive than trabecular bone. About 10%of the the treatment of a reduced bone mass in the cortical bone is remodeled each year. postmenopausal period. Trabecular (cancellous) bone is found in How to Acquire More Bone the axial skeleton, primarilyin the vertebral bodies (70%to 95%),with lesser concentra- Mechanical force plays an important role tions in areas such as the neck of the femur in bone formation and function, but it is not (25% to 35%) and the distal radius (5% to known how much exercise is needed and 20%). The remodeling process is far more whether there is an optimal form of exercise active in trabecular bone, in part because for bone accrual. It has been postulated16 the architectural arrangement of the bone that there is a physiologic \"band\" ofactivity plates provides a larger exposed surface that is site-specific:immobilization can lead area for exchange with the extracellular to severe bone loss at some sites, whereas compartment. Approximately 40%of trabec- repeated loading at appropriate strain mag- ular bone is remodeled each year. Because nitudes can result in bone hypertrophy.The of this greater activity, vertebral osteopo- frequency and degree of activity is impor- rosis occurs more frequently than hip (cor- tant: repeated and prolonged exercise tical-related) fractures. It may also account causes bone fatigue and microscopic frac- for the increased susceptibility of the ver- tures.16 Given appropriate intervals between tebrae to the bone mineral loss noted in fe- periods of exercise, however, normal bone male long-distance runners.14 turnover will repair these microfractures and even strengthen the bone.16 Excessive After longitudinal bone growth has been activity is known to have an adverse effect, completed, the bone mineral content and with stress fractures a common reality in mass of bone further increase until about long-distancerunners.16 the age of 35 years, at which point the indi- vidual is said to have achieved her maximal Gravity. Bone mineral is lost with the in- cortical bone mass. From this age until the activity of simple bed rest. The average rate onset of menopause, it is considered normal appears to be 4%per month during the early for women to lose at least 0.12% of cortical phase of bed rest; although subjects with bone per year (as measured by single- and higher initial bone mass lose bone more rap- dual-photon absorptiometry); after meno- idly than those with lower values, all immo- pause and until age 65, the rate of bone loss bilized patients seem to end up with a simi- increases to at least 1% per year, slowing lar bone mass.17 Lack of force on bones plays down after age 65 to 0.18% per year. This a major role in bone loss, with trabecular \"physiologic\" bone loss averages out to a bone being more sensitive than cortical 25% decrease in cortical bone mass over the
192 Developmental Phases bone. Three hours a day of quiet standing is Age. Age is yet another significant factor: partially effective in restoring bone mineral, bone mass accrual occurs more readily in while 4 hours of walking prevents the bone \"growing\" than in \"mature\" bone.21 Both an- loss associated with 20 hours of bed rest. imal experimentation and clinical experi- ence have shown that the accumulationof Osteogenesis in long bones requires me- appropriate mechanical damage can stimu- chanical stress; when electrodes are placed late bone hypertrophy. This requires the ex- on opposite sides of bone, bending results in posure of adult bone to cyclic strain levelsof a negative electrical potential on the con- 2000 microstrain or more.22 However, there cave side relative to the convex side.18 The is an optimal level beyond which increasing resulting piezoelectricity stimulates new strain levels will no longer enhance bone bone cell growth. It is therefore not surpris- mass and may even have a negative effect.22 ing that isometric or horizontal exercise— Thus, the type and intensity of exercise pre- which does not \"bend\" bone and thereby scribed must be tailored to the age of the in- stimulate this piezoelectricity—isnot able dividual. to restore bone loss associated with immo- bilization. Exercise Prescription. In presenting an osteogenic exercise program, twoadditional Systemic versus Local Effect. It is impor- criteria should be met: (1) the activity tant to differentiate the amount of exercise should be diverse and vigorous, but nonre- needed to maintain bone mass from that petitive,23 and (2) the exercise program needed to increase it. This difference is well should be enjoyable, in order to ensure illustrated by a study that compared male long-term compliance. In addition, a pro- professional tennis players with age- gram that will simultaneously improve car- matched casual tennis players. The former diovascular fitness would provide an added group was found to have an overall greater incentive and advantage. By extrapolating bone mass, but in addition, the cortical from animal data,24 it has been suggested thickness in the playing arm of the profes- that aerobic exercise at an intensity associ- sional tennis players was 34.9% greater than ated with 65% to 80% of maximal heart rate in the nondominant arm. The same was is osteogenic. found in female professional tennis players; cortical thickness in the dominant arm was Exercise and Osteogenesis: 28.4% greater than in the nondominant Clinical Research arm.19 Exercise thus seems to have both a systemic and a local effect and appears to be Several investigators have studied the ef- related to the type of exercise performed. fects of exercise programs upon bone min- When combined with the effect of gravity, eral density in postmenopausal women, weight-bearing activity is more osteogenic using various protocols for exercise. Some than weight-supported exercises such as of these studies have included hormone re- swimming. However, both male and female placement therapy in the protocol, and swimmers have been shown to have greater some have also quantified calcium intake. vertebral bone mineral content than do Disparate results reflect differences in pro- their sedentary counterparts of the same tocols and populations. sex.20 Although the differences between male swimmers and sedentary men were When interpreting the efficacy of a given statistically significant, the differences be- program, the method of bone strength mea- tween female swimmers and sedentary surement needs to be considered. Most women did not achieve significance, proba- assessments are based on radiologic tech- bly because of the smaller numbers of niques, single- and dual-photon absorp- women studied (58 male swimmers, 78 sed- tiometry, and/or CT scanning. Aqualitative entary men; 35 female swimmers,20 seden- improvement in bone strength resulting tary women). from aerobic exercise may also derive from
Menopause 193 an engineering rather than a biologic prin- entary controls (mean age 39.6 ± 1.0 years). ciple—an increase in bone width. Radial ex- Mean values of the mineral content and the pansion of long bones is an important deter- bone density of the marathon runners' ra- minant of bone strength. The so-called dial midshaft and middle phalanx (repre- cross-sectional moment of inertia (CSMI) is sentative of cortical bone) were significantly what determines bone's resistance to bend- greater, but the mean density of the os calcis ing. An increase in the external diameterof (trabecular bone) was higher in the physi- the bone, brought about by increased peri- cally inactive women.28 Women with mod- osteal (outer layer) new bone formation, can erate exercise had greater cortical but less compensate for the inevitable loss in the trabecular bone mineral contents, indicat- quality of bone tissue that occurs with aging. ing that the increase in cortical bone Cavanaugh and Cann25 have demonstrated through exercise came at the \"expense\" of that a moderate brisk walking program of 1 trabecular bone. year's duration does not prevent loss of ver- tebral bone density in early postmeno- Although anatomically distinct, the meta- pausal women. Kirk and colleagues26 re- bolic functions of the cortical and trabecular ported similar vertebral bone densities for bone compartments are shared—a gain in postmenopausal runners and age-matched one compartment may be matched by a loss sedentary women. Althoughthe calcium in- in another. These two studies raise the ques- take of the runners was higher (1145 mg/d tion: can one exercise too much, and if so, versus 707 mg/d), neither group consumed will this result in a compromise of the tra- adequate amounts by current standards. becular skeleton? Hypoestrogenic, amenor- These data suggest that exercise cannot rheic runners have been shown to have a re- compensate for an estrogen deficiency in duced amount of trabecular bone in their preventing bone loss. lumbar vertebrae (as measured by dual- photon absorptiometry) but normal or min- Relatively brief exercise programs have imally reduced cortical bone (as measured been shown to have a positive effect on ver- by single-photon absorptiometry and radi- tebral bone mineral.Sixteen healthy women ogrammetry).14,29-31 Lower bone density in (mean age 61 ± 6 years) participated in an these women correlates with estrogen defi- exercise program that involved walking, ciency, inadequate dietary calcium, and re- running, and calisthenics for 1 hour twice duced body weight. Calcium intake obvi- weekly. At the end of 8 months, the vertebral ously plays a very important role. When bone mineral content (measured by dual- reported, calcium intake was inadequate in photon absorptiometry) increased by 3%to most osteopenic groups, regardless of estro- 5%, whereas in an age-matched control gen and exercise status. The menstruating group it decreased by 2.7%. The bone min- marathon runners referred to previously eral content of the distal radius, however, lost trabecular bone despite an intact hypo- showed an average decrease of 3.5%.27 The thalamic pituitary ovarian axis; another authors concluded that physical exercise in- study has shown that physically active hibits or reverses bone loss from the lumbar women with anorexia nervosa (all of whom vertebrae in normal women, but that the were amenorrheic and obviously hypoes- changes in the forearm were independentof trogenic) had significantly greater bone these exercises. mass than a similar group of inactive ano- rectics.32 These results are divergent from another study that examined bone mineralization by Unpublished results from a study at the x-ray densitometry (middle phalanx of the Center for Climacteric Studiescomparingdif- fifth finger and os calcis) and photon ab- ferent forms of exercise in natural and sur- sorptiometry (distal and midshaft) in 42 gically menopausal women reflect on some normally menstruating marathon runners of the aforementioned issues—age, type and (mean age 37.7 ± 0.82 years) and 38 sed- intensity of exercise, and an \"intact\" estro-
194 Developmental Phases gen milieu. Bone mineral content in this Figure 11-3. Percentage change (mean ± SEM)in the study was measured by dual-photon absorp- bone mineral density (BMD) of surgical menopausal tiometry of the total skeleton. Naturally women after 1 year of hormone therapy alone (H) or menopausal women participating in aerobic hormone therapy plus Nautilus exercise (H + N). The (walking on a treadmill, riding a stationary probability (one-tailed t-test) associated with the bicycle) and muscle-strengthening (Nauti- change in spine BMDmeasures within the exercising lus) exercises, none of whom were receiving group wasp = 0.002. The probability(one-tailed t-test) hormonal therapy, had less bone loss over a associated with the change in spine BMD measures 1-year period than did a control group that within the hormone-only group was p = 0.44. Changes did not exercise. The controls lost 9.9% of between groups were not significant. (From Notelovitz their bone mineral content, compared with et al,35 p 587, with permission.) 3.8% in the Nautilus exercise group and 0.5% in the bicycle-riding group. The treadmill Exercise and Calcium Intake subjects gained 0.4%.33 The precise mechanism whereby exercise Heikkinen and associates34 showed that stimulates new bone formation is not clearly weight trainingfor 40 minutes in one session established. Mechanical load, muscular ac- per week was insufficient to enhance the tivity, and gravity serve as extracellular beneficial effect of estrogen and progesto- stimuli that are transmitted to bone cells to gen on bone mineral density in postmeno- initiate their genetic program for growth pausal women, nor was there any improve- and differentiation. Intermediaries include ment in bone density in a control group not events such as the generation of piezoelec- treated with hormonal therapy. However, a tricity, which stimulates cyclic nucleotide study performed at the Center for Climac- teric Studies demonstrated increased bone Table 11-1. EFFECT OF EXERCISE AND mineral density of the spine when a groupof HORMONE REPLACEMENT THERAPYON surgically menopausal women were treated BONE MASS IN POSTMENOPAUSAL with both estrogen and intense Nautilus WOMEN weight trainingfor 45 to 60 min/wk, divided into three sessions.35 In this study, the in- HRT* Moderate Intense Effect on crease in vertebral bone mineral density Exercise Exercise Bone Mass (measured by dual-photon absorptiometry) (Aerobic) (Nautilus) was statistically significant for the estrogen- plus-Nautilus group, compared to baseline, No Yes Yes 0 but the increase did not reach statistical sig- No Yes 0 nificance for the estrogen-only group, or for Yes + the between-group comparison (Fig. 11-3). It is likely that this lack of significance re- 'Hormone replacement therapy. sulted from the small numbers studied (n = Source: From Notelovitz et al,33 with permission. 9 for estrogen plus Nautilus; n = 11 for es- trogen only). All subjects ingested a mini- mum of 1400 mg of calcium daily during the 12-month study. These studies suggest that an estrogen-replete state might be needed for an osteogenic effect in women involved in intense exercise programs, and that more moderate levels of activity can conserve and maintain bone independent of the estrogen milieu (Table 11-1). However, more studies are needed to delineate the frequency, in- tensity, and duration of exercise necessary.
Menopause 195 activity, prostaglandin synthesis, and other by exercise, the bone may not improve in matrix-derived bone growth factors. strength in response to stress because their continuity (and hence structural integrity) It has been established that exercise is di- has been lost. Nevertheless, light to moder- rectly associated with the laying down of ate exercise in older women has resulted in matrix on the remodeling surface of bone's an improvement of the cortical bone mass. trabeculae and cortices. The matrix is com- Smith and co-workers38 designed an exer- posed primarily of collagen. Chvapil and cise program for older women (mean age 81 colleagues36 showed that the amount and years) that oriented activity (1.5 to 3.0METs concentration of collagen in the femurs of in intensity) around a chair. (One MET adult rats increased with exercise, but there equals an oxygen uptake of 3.5 mL-min\"1- was no effect on the calcium content. This kg\"1, the average value of effort during chair experiment illustrates a most important rest.) Over 3 years, the exercise group dem- point: to benefit from exercise and its osteo- onstrated a 2.9% increase in midshaft radius genic stimulus, it is necessary to ensure an bone mineral content, whereas a matched, adequate supply of the substrate (mainly nonexercising control group showed a calcium) needed to mineralize and mature 3.29% decrease. the newly formed bone. It is well known that fluoride therapy without simultaneous cal- Inadequate attention is given to the pre- cium supplementation will increase miner- scription of exercise for women with estab- alization of the axial skeleton, but at the ex- lished osteoporosis, most of whom will pense of the cortical bone and with an present to the physician during the late cli- increase in hip fractures.37 A similar situa- macteric. Key is discouraging activities that tion may be true for exercise-induced osteo- involve flexion of the back. Long-term fol- genesis, except that in this instance it is the low-up of patients with radiologically con- cortical bone that benefits at the expense of firmed osteoporosis revealed concurrent the trabecular compartment. This may fractures in 16% of women practicing back prove to be one of the reasons why the extension exercises, 89% in a flexion pro- amenorrheic women reported by Drinkwa- gram, 53%in a combined extension and flex- ter and associates14 had lower spinal, but not ion regimen, and 67% in a nonexercising cortical, bone mineral content when com- control group.39 Posture is also important. pared with the eumenorrheic controls. Al- Avoidance of flexion during sedentary activ- though both groups met the current recom- ities, such as sewing, can prevent further mended dietary allowance of 800 mg of stress on already weakened vertebrae.40 In- elemental calcium per day, the amenorrheic struction should also be given to avoid back subjects fell short of the recommended straining by twisting, lifting, and making amount needed to maintain calcium balance sudden, forceful movements. To remove the in low estrogen states (1500 mg), whereas strain from the lower back when lifting or the eumenorrheic women exceeded their reaching lower objects, the large muscles of daily requirement of 800 mg. the legs (i.e., the hamstrings and quadri- ceps) should be used, by bending the knees Established Osteoporosis and keeping the back vertical during these activities. Exercise in women with established os- teoporosis has to be modulated because Walking is the safest form of exercise for pre-existing microfractures and discontinu- women with osteoporosis. Also safe and ef- ity between the trabecular plates, especially fective are group activities such as square in the axial skeleton, may be aggravated by dancing, ballroom dancing, and folk danc- weight-bearing exercise. Furthermore, even ing, as well as other activities such as riding though individualfragments of the horizon- a three-wheel bike or an exercycle. Swim- tal trabecular plates may be hypertrophied ming is an excellent exercise that allows pa- tients to regain their confidence in being
196 Developmental Phases physically active, and at the same time al- the atherogenic process.45 Exercise has a lows them to increase the flexibility and mo- beneficial effect on the lipoprotein moiety, bility of their joints. Osteoporotic or mark- especially regarding the HDL cholesterol.46 edly osteopenic women should be advised to avoid activities such as aerobic (jazz) Physical inactivity has also been linked to dance classes that jar the spine and empha- atherogenic disease. Men who are physi- size flexibility. In evaluating these women, cally active have fewer stigmata of coronary care should be taken to test for balance and heart disease, and when they do occur, they for orthostatic hypotension, and to advise are less severe and appear at an older age.47 them about practical measures such as the The same is true for women.48 Despite some type of shoes they wear. previous claims that physical inactivitycon- tributed only indirectly to cardiovascular Additional information about bone con- disease risk, there is now considerable evi- cerns may be found in Chapter 5. dence that low physical fitness stands as an independent risk factor, in both men and ATHEROGENIC DISEASE AND women, for all-cause mortality, cardiovas- CARDIORESPIRATORY FITNESS cular disease mortality, and cancer mortal- ity.49,50 In addition to the direct role demon- Premature cessation of ovarian function strated after controlling for other known has been shown to increase the risk of myo- risk factors,50 regular physical exercise cardial infarction. Women who had a bilat- probably also plays an indirect role by re- eral oophorectorny before age 35 were esti- ducing other known risk factors for coro- mated to have a 7.2 times greater risk of nary heart disease, such as serum lipid con- being hospitalized for a myocardial infarc- centrations and ratios,51 hypertension,51 tion than age-matched normal premeno- hyperinsulinemia,52 diabetes mellitus,51,53,54 pausal women.41Other studies have also ob- and abdominal fat.55,56 The type, intensity, served high rates of coronary disease in and duration of exercise linked to a potential women who experience an early meno- decrease in coronary heart disease varies. pause.7,42,43 There is a general consensus that There appears to be a threshold of activity the postmenopausal period is associated needed to achieve a benefit. This has been with well-defined high-risk factors for ath- estimated to be 300kcal/d above normal ac- erogenesis: increased total plasma choles- tivity and requires 30 to 60 minutes of mod- terol and increased low-density lipoprotein erately intensive exercise per day.57 Earlier (LDL) levels.7 This is a biologic, not a chron- speculation that women,58 especially older ologic, event. A Swedish study compared women, would not be able to achieve this women aged 50 and older, of whom some goal has been disproved. were still menstruating and others had reached menopause; serum cholesterol and Based on the previous observations, two triglycerides were significantly higher in the practical aspects of physical activity and postmenopausal group, and these levels in- cardiovascular health can be objectively creased with postmenopausal age.44 measured: (1) the response of biochemical parameters such as cholesterol and HDL The pathogenesis of atherosclerosis is cholesterol, and (2) measures of physical characterized by two factors: (1) endothe- fitness and exercise quantity—maximal ox- lial desquamation with later smooth muscle ygen uptake (Vo2max) and total exercise cell proliferation, and (2) cholesterol depo- time. sition within these cells. Inhibition of LDL internalization and deposition in the Lipids, Lipoprotefns, and smooth muscle cell by high-density lipopro- Exercise teins (HDL) cholesterol is said to be a key factor in the prevention or slowing down of The plasma lipoproteins are the means whereby endogenous synthesized lipids are
Menopause 197 transported in the circulation.They are clas- cussion group served as the controls. Levels sified according to their gravitational den- of serum cholesterol, triglycerides, total sity into four basic classes: chylomicrons, HDL, and HDL2a and HDL2b were monitored very low density lipoproteins (VLDL), LDL, at baseline, at 6 weeks, and at 12weeks. The and HDL. The latter are frequently subfrac- exercise groups were instructed to walk-jog tionated into HDL2 and the more dense for 30 minutes (after a 15-minute warm-up hHiDgLh3e.rTinhewoHmDeLn259cahnodleissteinrovlersceolmy preolnaetendt is session) and to pace their activity in order to to maintain their heart rate at 70% to 80% of the development of coronary heart dis- their predicted maximum heart rate. Oneex- ease.60 Exercise stimulates HDL2, which is ercise session each week was supervised by higher in both male and female runners than a group therapy leader, and the women ex- in sedentary controls. In one study, for ex- ercised on their own during two other ses- ample, male runners had HDL2 cholesterol sions per week. Cardiorespiratory function values of 119versus 53 mg/dL for sedentary was determined at baseline and at 12weeks men; in women the values for active and sed- by having subjects walk on a motorized entary subjects were 218versus 122 mg/dL.59 treadmill until they declared fatigue or The HDL-elevating effect of exercise is reached their predicted maximal heart rate. thought to be due to an increase in lipopro- The exercising group had a significantly tein lipase, an enzyme responsible for the greater increase in Vo2max, time spent on catabolism of triglyceride-rich lipoproteins. the treadmill, and time required to attain Lipoprotein lipase is found in greater con- 90% of maximal oxygen consumption (p < centrations in the skeletal muscle fibers 0.01), but did not show a statistically signif- (slow-twitch) of endurance athletes.61 icant difference in the lipid or lipoprotein The adverse effects of estrogen deficiency fractions at either 6 or 12 weeks.64 This dis- on low-density lipoprotein cholesterol lev- appointing result was confirmed by Franklin els tend to be offset by aerobic training. and associates,65 who exercised their sub- However, the beneficial effects of strenuous jects four times a week as part of a 12-week exercise on plasma apolipoprotein levels conditioning program. These discrepant re- can be reversed, in premenopausal women, sults may be explained by the duration of by exercise-induced amenorrhea and de- the exercise program and intensityof the ex- creased serum estradiol levels.62 ercise. For example, when the weekly run- Table 11-2 lists the serum cholesterol val- ning mileage of 22 women was increased ues found in a cross-sectional study of from 3.5 miles to 44.9 miles (over a7-month women conducted at the Center for Climac- period), their mean HDL cholesterol in- teric Studies, showing an age- and meno- creased from 53.5 to 58.5 mg/dL (p < 0.01).66 pause-related increase.63 To determine whether this change would be improved by In another study, hysterectomized post- exercise, a group of 50 healthy women be- menopausal women who exercised thrice tween the ages of 40 and 65 were invited to weekly in 30-minutesessions of aerobic ex- participate in a 12-week program of exer- ercise at a minimum of 70% of maximalheart cise, discussion sessions, or both. The dis- rate had a significant reduction in total serum cholesterol and LDL cholesterol. Table 11-2. SERUM CHOLESTEROL (mg/dL) OF WOMEN, RELATED TO AGEAND MENOPAUSE Premenopausal Postmenopausal Age range 35-45 46-55 46-55 56-65 66-75 N 30 24 23 24 10 Cholesterol (mean ± SEM) Source: From Notelovitz et al.6: 170.5 ± 4.3 203.2 ± 7.6 233.8 ± 5.9 230.1 ± 6.9 238.8 ± 6.7
198 Developmental Phases However, this effect was not greater than with age, especially after age 50. Women that induced by oral estrogen alone.67 usually achieve maximal Vo2max values in their 20s; by age 50 to 65 years, the values Like their younger counterparts, post- are decreased by almost 30%.74 This loss of menopausal women who engage in regular aerobic power is not related to menopause endurance exercise have higher HDL cho- per se, however. In a recent study, women lesterol levels than inactive women.68-70 aged 45 to 55 had their Vo2max predicted by Postmenopausal long-distance runners and means of a submaximal bicycle ergometer joggers had significantly greater levels of test.73 They were divided into premeno- HDL cholesterol compared with a control pausal and postmenopausal groups, as con- group of relatively inactive women—79.8, firmed by hormonal analysis and by their 73.5, and 61.8 mg/dL, respectively. The menstrual pattern: postmenopausal women lipid-lipoprotein profiles were minimally af- were required to have been amenorrheicfor fected by exercise in a simultaneously stud- at least 1 year. As reflected in Table 11-3, ied group of exercising premenopausal serum LH and FSHwere significantly higher women,70 raising the issue of whether it is in the postmenopausal women (p < 0.0001), possible to make \"normal\" more normal. and the estradiol and estrone levels were significantly lower (p < 0.0001). The pre- It appears that the cardioprotective HDL menopausal women were slightly younger cholesterol level improves after only 3 (48.7 ± 0.4years versus 52.2 ± 0.4), but the months of moderate activity (e.g., running difference was not statistically significant. 10 to 15 miles/wk) or low-level activity (e.g., No significant difference was found in the es- walking 30 miles/wk).59 As with men, exer- timated Vo2max for the two groups (p > cise training in women lowers total choles- 0.05).73 terol slightlyor not at all.65,66 The observed decline in Vo2max with age probably reflects a loss of functional capac- Aerobic Power ity due both to a natural age-related deteri- With the advent of the \"fitness craze,\" oration and to a decrease in physical activity. The age-associated reduction in women have come into their own and have cardiorespiratory efficiency at submaximal exploded the myth that women are \"frail\"; exercise, however, is due primarily to physical fitness in young women has now weight gain rather than to actual systems de- become socially acceptable and, in many generation.75 The rate of decline is slower in circles, even desirable. Until fairly recently, however, it was felt that exercise would not Table 11-3. MEAN ESTIMATED MAXIMAL benefit middle-aged people, and that the de- O2 UPTAKE VALUESAND HORMONAL cline in cardiorespiratory function with STATUS (± SD) OF PREMENOPAUSAL aging would reduce the expected benefit AND POSTMENOPAUSAL WOMEN AGE 46- from exercise.58 Furthermore, it was postu- 55 YR lated that menopause per se could be re- sponsible for the decrease in aerobic power Parameter Premeno- Postmeno- in women over the age of 50.71,72 pausal pausal (n = 28) (n = 30) As with men, cardiorespiratory fitness does decrease with age, but this decline is Es(timmLa-tekdg V- 1 'o-2mmianx- 1 ) 27.4 ± 6.3 26.3 ± 4.7 not related to the hormonal changes of the LH (mlU/mL) 23.5 ± 3.6 62.8 ± 3.5 climacteric. Figure 11-4 shows that a dec- FSH (mlU/mL) 12.6 ± 2.6 55.7 ± 3.5 rement of 5.5% of Vo2max occurred with Estrone (pg/mL) 107.5 ± 11.5 62.9 ± 3.9 each succeeding decade between ages 35 Estradiol (pg/mL) 146.2 ± 18.7 19.5 ± 3.5 and 75 in a study of 163 healthy sedentary women.73 This observation approximates Source: From Notelovitz et al,73 with permission. with the generalization that sedentary indi- viduals have a 1% loss of Vo2max per year
Menopause 199 Figure 11 -4. Measured 1V2o-2lmeaadxE(mCGL • kg • min) in 163 healthy climactericwomen, who first were screened for cardio- vascular normalcy by a stress test and physical examination.The Vo2max was elicited using a modified Balke treadmill procedure, and was directly measured using a Beckman Metabolic MeasurementCart. (From No- telovitz et al.,73 with permission.) phrysically active men76 and women.76,77This times a week for 12weeks) resulted in a sig- raises the issue of whether menopausal nificant increase in maximal oxygen con- women can be efficiently trained. Premeno- sumption, time on the treadmill, and the pausal women (mean age 41 years) who time to reach 90% of maximal oxygen con- trained for 9 weeks improved their Vo2max sumption, when compared with age- by 12.1%, while similarly trained postmeno- matched female controls who did not exer- pausal women (mean age 57 years) im- cise.80 More recently, 63 postmenopausal proved their Vo2max by 19%.78 This result women were evaluated over a 1-year period, has been confirmed by others,79 including during a structured program that involved two studies conducted at the Center for Cli- three weekly 20-minute treadmill, ergome- macteric Studies in Gainesville, Florida. ter, or Nautilus (muscle-strengthening) ses- Moderate exercise (walk-jogging three sions. Two nonexercising groups were
200 Developmental Phases Table 11-4. RESPONSE OF CLIMACTERIC WOMEN—MEANAGE 56 YR—TO INTENSIVE STRUCTURED EXERCISE,81 MEAN (± SD) MAXIMAL O2 UPTAKE (mL-kg-'-mirT1) Group Age n Baseline 3 Mo 6 Mo 12 Mo % Difference Baseline vs 12 Mo Nautilus 59.3 ± 6.7 13 26.0 ± 5.2 26.1 ± 4.7 26.5 + 4.0 26.2 ± 3.9 0.8 Treadmill 54.9 ± 6.9 10 27.1 ± 2.7 29.5 ± 2.8 30.5 + 2.8 29.5 ± 2.4 8.9 Ergometer 55.9 ± 6.9 10 26.7 ± 4.7 28.9 ± 4.1 30.2 ± 4.1 30.0 ± 4.8 12.4 Control 62.0 ± 7.1 14 26.5 ± 4.7 26.1 ± 6.0 25.9 ± 5.9 26.2 ± 5.8 -1.1 Hormone 48.4 ± 7.2 16 26.6 ± 3.9 26.3 ± 3.7 26.4 ± 4.2 25.1 ± 3.9 -5.6 Source: From Notelovitz et al,81 with permission. included: an age-matched nontreatment Cowan and Gregory78 noted a 29.6% increase group and a slightly younger group onhor- in total walking time; in the Gainesville mone replacement therapy. Aerobically study,81 the time for treadmill walkers in- trained subjects were exercised at 70% to creased 21.5%, and for bicyclists, 17.4%. Pre- 85% of the maximal heart rate. Significant menopausal women exposed to the same ex- improvements in both Vo2max and time on ercise regimen had an improvement rate of the treadmillwere recorded and maintained 10.9% in total exercise time.78Sincethe heart only by the bicycle and treadmill groups rate and stroke volume response to exercise (Tables 11-4and 11-5).81 was appropriate in postmenopausal women, The anticipated degree of improvementin there is a possibility that the lesser percent- aerobic power is inversely related to the age response in Vo2max compared with per- subject's initial level of fitness, but at all ini- centage improvement in exercise timemight tial levels, the greater the intensity and fre- be accounted for by partially compromised quency of the training program, the greater lung ventilation, lung diffusion capacity for the improvement. For example, the post- oxygen, and/or oxygen utilization by thetis- menopausal women in Cowan and Gregory's sues in the postmenopausal period. study78 had a 19% improvement in VLo. k2mga-x1 (from 1 2.6 mL.kg- 1.min-1 to IS .m Less attention has been directed to older min-1). compared with a 10.7% improve- women. When 10 healthy women of mean ment in the Gainesville study31 (from 26.9 age 72.0years exercised three times per mL-kg-1-min-1to29.8mL-kg-1-min-1). week for 20 minutes per session, at 70%of An intriguing observation in both of these maximum heart rate, for 26 weeks, maxi- studies is the considerably greater improve- mum oxygen uptake increased 8.4% and ment in total exercise time versus Vo2max. total exercise time increased 25.4%, com- pared to a 6.1%decrease in maximum oxy- Table 11-5. RESPONSE OF CLIMACTERIC WOMEN—MEAN AGE 56 YR—TO INTENSIVE STRUCTURED EXERCISE,81MEAN (±SD) TOTAL EXERCISETIME (MIN) Group Age n Baseline 3Mo 6 Mo 12 Mo % Difference Baseline vs. 12 Mo Nautilus 59.3 ± 6.7 13 12.1 ± 3.2 12.2 ± 2.5 12.9 ± 2.4 12.5 ± 2.4 5.3 Treadmill 54.9 ± 6.9 10 12.5 ± 1.6 14.2 ± 2.1 15.2 ± 2.0 15.3 ± 2.1 21.5 Ergometer 55.9 ± 7.9 10 13.0 ± 3.1 14.1 ± 3.0 14.5 ± 3.0 15.2 ± 3.3 17.4 Control 62.0 ± 7.1 14 12.2 ± 3.3 11.6 ± 3.6 12.2 ± 4.0 12.1 ± 3.4 -0.95 Hormones 48.4 ± 7.2 16 13.4 ± 2.4 12.6 ± 2.3 13.0 ± 2.3 12.3 ± 2.2 -7.7 Source: From Notelovitz et al,81 with permission.
Menopause 201 Table 11-6. IMPROVEMENT OF MAXIMAL O2 UPTAKE FOLLOWING AEROBIC TRAINING PROGRAMS IN WOMEN OVER AGE 50 Author Duration of Frequency Intensity Duration of %Gain in Exercise of Exercise of Exercise Training Maximal per Session per Week Program O2 Uptake n (min) 2-3 70%* (wk) 3 85% 8 Kilbom58 13 30 4 7 20.8 Adams and 17 50 3 120-150 12 >30 60 4 60-80% 7 17 DeVries133 25 55 3 14 18.9 Sidney etal.134 28 50 3 80% 9 8.9 Sidney and 20 3 52 12.4 14 20 70-85% 52 8.4 Shephard135 20 70-85% 24 Cowan and 10 (T) 70% 10 (E) Gregory78 10 Notelovitz et al81 Probart et al82 *Vo2max. Maximum heart rate. Heart rate. T = treadmill; E = ergometer. Source: Adapted from Cowan and Gregory.78 gen uptake and a 5.4% decrease in total ex- other cross-sectional study,83 active women ercise time in six age-matched controls who had a fitness gain of one decade when com- did not exercise.82 These data and others pared to sedentary women. The mean (Table 11-6) indicate that older women can Vo2max of active 40- to 49-year-old women certainly expect to improve fitness and ex- was higher than sedentary 30-to 39-year-old ercise capacity with aerobic training. women; active 50-to 59-year-old women had values similar to sedentary women in their In the studies summarized in Table 11-6, 40s. One way of encouraging women to ex- the percentage gain in aerobic power ranges ercise is to use cardiorespiratory fitness as- from 8% to 30%. With only one exception, sessments as a means of demonstrating im- the duration of these training programs was provement in aerobic function before the less than 14 weeks. The best improvement physical benefits of exercise are appreci- was obtained in programs whose durationof ated. Bruce and colleagues84 reported that exercise exceeded 30 minutes in each ses- 63% of their patients attributed a change in sion. The study that continued for 12 one or more adverse health habits to a months demonstrated that most of the im- graded exercise test. Persons with an abnor- provement attained by 12 months had been mal result were motivated the most. achieved by 3 months of training. These re- sults, however, do not reflect the true poten- Maximal oxygen uptake tests need to be tial of older women engaged in long-term, performed in a specially equipped labora- intensive exercise programs, nor do they tory and are not suited to everyday clinical consider a most important practical, real- practice. Submaximal testing, on the other life issue of exercise: compliance. hand, is more suited to the practicing phy- sician. Several studies have shown that pre- Measurements of aerobic fitness may help dicted maximum Vo2 values (using a bicycle to motivate some sedentary women. Kirk ergometer) correlate well with observed and co-workers26 reported higher levels of maximal testing when corrected for age,85,86 fitness (maximal oxygen consumption) but none of these studies have involved cli- among postmenopausal runners compared macteric women. To test this relationship in to age-matched sedentary women. In an-
202 Developmental Phases postmenopausal women, 29 women (mean diorespiratory fitness for women (Table 11- age 55.6 ±9.1 years) participating in an on- 7), potential exercise candidates can obtain going exercise program had both amaximal a good index of both their current fitness treadmill test and a submaximal ergometry status and the goals they should reach. Be- test.73 The interval between the two tests cause postmenopausal women appear to was less than 1 month, and the order of test- show a greater response to a given exercise ing was randomly selected. The measured program in total exercise time than in max- Vo2max was 28.6 ± 4.9 m L . k g - 1 - m i n - 1 , and imum oxygen uptake, the total exercise no- the -p1r.eWdihcteendthVeol2amttaexr 32.5 ± 5.3 mL-kg~'- mogram (Fig. 11-7) may be used as the pri- min result was calculated mary indicator of exercise response and using the recommended Astrand age correc- improvement. tion factor, the mean mpriend-1i.ctTedhisVoco2mrraexlawteads 23.4 ± 4.9 mL -kg-1 In view of the laziness inherent in most closely with the directly measured result (r people, any program that can produce im- = 0.789; Fig. 11-5). proved results for little effort is more likely Submaximal testing can thus be used both to be successful and lead to a greater degree as a screen to determine the cardiorespira- of compliance than a program that requires tory fitness of climacteric women and as a great effort and discipline. Schoenfeld and way of monitoring the response to pre- co-workers87 examined the efficiency of scribed exercise. Patients at high risk for walking with a backpack load as a method cardiovascular disease and those classified for improving physical fitness of sedentary as having fair to poor fitness (as measured men. They showed that it was possible to in- by ergometry) require more detailed evalu- crease Vo2max by 15%to 30% by walking for ation before embarkingon a prescribed ex- 3 to 4 miles with a 3- or 6-kgbackpack. When ercise program. A nomogram is also very we compared the effects of treadmill walking useful (Figs. 11-6 and 11-7); when used to- with and without extra weight in a small gether with age-adjusted tables listing car- group of postmenopausal women, we found greater improvement in the aerobic capacity of the load-bearing group.88 However, con- firmatory studies with larger numbers are needed to determine whether load-bearing enhances the efficacy of aerobic training or modifies the perceived effort. Figure 11-5. Correlation between measured and pre- MUSCLE TISSUE AND dali.c,7t3edwVitho2mpaexrimn icslsiimonac.)tericwomen. (From Notelovitz et STRENGTH Age-Related Loss of Muscle Tissue and Strength Muscle mass and muscle strength decline with aging, and muscle weakness can greatly reduce the qualityof life and self-sufficiency of many older women. The age-related de- cline in lean body mass correlates with sev- eral changes: a decline in endogenous growth hormone (GH),89 a decline in pitu- itary responsiveness to growth hormone re- leasing hormone (GHRH),90 loss of muscle fibers,91 neuromuscular alterations, inactiv-
Menopause 203 Figure 1M1-,6F.ieNldosrmC,aetitvael:VUon2mpuaxblvisahlueedsdfaotra.cClimenatcetrefroicr women. Mean ± 1 and 2 SD for each age group. (From No- telovitz Climacteric Studies, Gainesville, FL, with permission.) ity, and other age-related changes. Pre- Table 11-7. GUIDELINESFOR FITNESS menopausal women have significantly ASSESSMENT BY Vo2max ( m L - k g - 1 m i n - 1 ) greater pituitary response to GHRH than do OF HEALTHY WOMEN AGE 30-70 men of the same age, but postmenopausal women do not;90 this finding suggests that Age Poor Fair Average Good Excellent postmenopausal estrogen deficiency accel- erates the age-related decline in GH secre- 30-39 <20 20-27 28-33 33-44 45 + tion and may also accelerate the loss of mus- 40-49 <17 17-23 24-30 31-41 42 + cle tissue that occurs as women age. 50-59 <15 15-20 21-27 28-37 38+ Although Rudman and his co-workers92 re- 60-69 <13 13-17 18-23 24-34 35 + ported that older men increased both lean body mass and skin thickness and de- Source: Adapted from Exercise Testing and Training in Apparently Healthy Individuals: A Handbook for Physicians, published by the Committee on Exercise, The American Heart Association, Dallas, TX, 1972.
204 Developmental Phases Figure 11-7. Normative total exercise time (.TET) to exhaustion values for climacteric women, using modified Balke method. Mean ± 1 and 2 SD for each age group. (From Notelovitz M, Fields C, et al: Unpublished data. Center for Climacteric Studies, Gainesville,FL,with permission.) creased adipose tissue mass during GH in terms of milliliters per kilogram per min- treatment, this has not been studied in older ute of muscle, as determined by 24-hour women. Furthermore, the safety of such urine creatinine measurements. Increasing therapy has not been demonstrated. muscle mass can thus play an important role in determining energy expenditure: a 2-kg Several cross-sectional studies also have increase in a woman's lean body mass re- shown a loss of muscle strength with age, sults in an additional expenditure of about beginning after the third decade of life and 50 kcal/d, the equivalent of about 5 Ib of amounting to a decline of 16.5% or more.93 body fat per year. The loss is greater in women.94 Loss of mus- cle tissue is related to a number of important Muscle is also an important determinant metabolic activities. For example, Tzanoff of carbohydrate utilization.The rate of glu- and Morris95 maintain that the decrease in cose removal from muscle is more rapid in muscle mass may be wholly responsible for physically active persons, and the amount of the age-related decrease in basal metabolic insulin needed is significantly reduced.96 rate (BMR). The average Vo2max of older This effect is reputed to be due to the en- men was 22% lower when compared with hanced sensitivity of insulin receptors in younger men, but this difference decreased skeletal (and adipose) tissue. Obesity and to only 8%when the values were expressed diabetes are two age-related conditions that
Menopause 205 are prevalent in the late climacteric. Van gens) will provide relief for most women. It Dam and colleagues96a have shown improve- should be noted that medroxyprogesterone ment in glucose tolerance among postmeno- acetate has not been approved, in the pausal women following aerobic exercise United States, for use in women with breast training. cancer. Strength Training OTHER AGE-RELATED Weight training in women has been shown CHANGES to improve strength with a loss of adipose Exercise and Adipose Tissue tissue and with relatively little muscle hy- Most people add adipose tissue with pertrophy. These studies have involved young women, trained athletes, or both, aging. There is no evidence that accumula- however.97-99 It is not known whether mus- tion of adipose tissue is related to meno- cle strengthening exercises will enhance the pause, estrogen deficiency, or any other al- metabolic function of postmenopausal skel- terations in reproductive hormones, but etal muscle, and if so, to what degree. Ex- many women first notice this accumulation trapolation from data collected in male sub- around the time of menopause. Menopause jects suggests that the accumulation of also has not been shown to affect the distri- greater mass will lead to greater energy ex- bution of body fat,105 but there is a progres- penditure. Strength training does not im- sive age-related increase in upper and cen- prove cardiorespiratory function (see Table tral body fat deposition, which tends to 11-4), a finding confirmed by studies done accelerate in postmenopausal women.106 in middle-aged men.100 Weight training However, it remains to be shown whether stresses muscles far more than do most aer- this change is related to menopause, aging, obic exercises. It is safe to start an aerobic or both. exercise program and then, many months later, to start lifting weights. Levels of adipose tissue lipoprotein lipase (LPL) correlate directly with body mass OTHER MENOPAUSAL index (in kilograms per square meter of PROBLEMS: VASOMOTOR body surface) and affect the maintenance of SYMPTOMS adipocyte size, body weight, and obesity.107 Adipocyte size is similar at mammary, ab- Very few studies have addressed the re- dominal, and femoral sites and is similar lationship between menopausal vasomotor for premenopausal and postmenopausal symptoms (\"hot flushes\") and exercise. In women.108 It has been shown108 that femoral one study, Hammar and co-workers101 found LPL activity is much higher among pre- vasomotor symptoms to be less common menopausal women than among postmeno- among exercising menopausal women than pausal women and that, among premeno- among inactive women. Since exercise has pausal women, it is much higher than it is at not been shown to relieve symptoms, how- mammary or abdominal locations. Treat- ever, this finding may reflect a self-selection ment of postmenopausal women with estra- bias, representing differences between the diol and a progestogen leads to an increase two groups questioned. in femoral LPL activity.109 When percutane- ous progesterone is applied to the femoral Although the etiology of the menopausal region of premenopausal women during the vasomotor flush remains enigmatic, estro- follicular phase of a natural menstrual cycle, gen remains the most effective form of ther- LPL activity rises locally.110These data sug- apy available.102 When estrogen is contrain- gest that progesterone is an important de- dicated, medroxyprogesterone acetate103 or terminant of femoral LPL activity.111 megestrol acetate104 (synthetic progesto- Regional fat distribution has achieved im-
206 Developmental Phases portance since it was demonstrated that ab- subchondral bone, cyst formation, and nar- dominal fat is a risk factor for cardiovascular rowing of the joint space. disease and diabetes, while femoral fat is not.55,56 Aerobic exercise facilitates the loss Postmenopausal women have decreased of abdominal fat more readily than fat at amounts of collagen in skin and bone,118 and other sites, and promotes fat loss more it is most likely that the same is true for the readily in men than in women.112-115 It isfor- collagen content of their articular surfaces. tunate that abdominal fat is so sensitive to The collagen in the skin (and possibly also exercise, since this facilitates reduction in in the bone) of postmenopausal women is disease risk. However, the relative resist- responsive to estrogen replacement. Al- ance of femoral fat depots to exercise may though arthralgia is a common symptom in discourage many women with a preponder- the late climacteric,a direct linkage between ance of femoral fat. menopause and joint disease has not been established. However, a study has demon- Inactivity is the most common cause of strated that noncontraceptive hormonal obesity, and it accelerates the accumulation therapy does help some women with rheu- of body fat that occurs naturally with aging. matoid arthritis.119 Cowan and Gregory78have reported a lossof body fat duringa 9-week trainingprogram in With the increased interest in jogging, a women, confirming that exercise can cer- question arises of whether damage to the tainly help older women to lose fat.Control musculoskeletal-articular system exceeds of weight and body fat is discussed more the benefit of exercise. Lane and asso- thoroughly in Chapter 2. ciates120 recently studied female long- distance runners over age 50 and compared Exercise and Osteoarthrosls them with age-matched nonactive commu- The articular cartilage that covers the nity controls. The female runners did have more sclerosis and spur formation in the bone ends in joints is rich in collagen and weight-bearing areas of the spine and knees, the mucopolysaccharide proteoglycan. This but not in the hands. These changes were collagen layer acts as a barrier preventing not found in men studied in the same and the leakage of proteoglycan from the deeper other investigations.121 layers into the joint space, and at the same time it inhibitspotential harmful enzymes in Given the asymptomatic nature of these the synovial fluid from perfusing into the changes and the difficulty of extrapolating deeper cartilage.116 Loss or damage to the cross-sectional data into \"real-life\" terms, it cartilage layer leads to joint degeneration cannot be concluded that jogging has an ad- and the development of osteoarthritis. verse effect on the joints of middle-aged women. The absence of joint changes in Osteoarthritis is a highly prevalent dis- age-matched and hormone-replete men, ease: 86% of women over the age of 65 show however, suggests the possibility that an es- radiologic evidence of the condition,117 al- trogen-primed articular surface (with an im- though only 25% to 30% of individualswith proved collagen content) might be similarly diagnosed osteoarthritis are symptomatic. resilient to mechanical stress. There are conflicting opinions regarding the role of microtrauma to the joint surface in EXERCISE AND WELL-BEING the pathogenesis of osteoarthritis. Impulse The administration of exogenous estro- loading causes trabecular microfracture with subsequent healing by sclerosis, result- gens, especially parenteral estrogen ther- ing in stiffened bone that increases the apy, to postmenopausal women is fre- stress on the articular cartilage, with even- quently associated with a mood-elevating tual damage to the cartilage and joint degen- effect. Exercise is also known to induce a eration. These changes appear on roentgen- state of well-being and, according to some ogram as osteophytes, sclerosis of the
Menopause 207 studies, a reduction in symptoms such as factors that contribute to a \"refreshing\" depression and anxiety. The early work of sleep period.129 Weber and Lee122 demonstrated that vigor- ous activity in animals had a positive influ- To evaluate the effect of exercise on psy- ence on psychologic measures and that this chologic well-being, preprogram and post- was probably due to alterations in brain program psychosocial measures were ob- neurotransmitter levels or activity, or tained by questionnaire and standardized both.123 Studies in humans have been less tests in a group of healthy women (age 40 to clear, and there is some question whether 64 years) participatingin a 12-week exercise the \"runner's high\" really exists.124 program. Methods of evaluation included a self-report of physical activity, a somatiza- Part of the controversy lies in the fact that tion scale, the multidimensional health much of the research has been conducted in locus of control inventory, the Profile of nondepressed subjects. Greist and col- Mood States Scale, and a social support leagues125 demonstrated that aerobic exer- questionnaire. Members of the exercised cise performed for 12 weeks reduced de- group were required to walk-jog for 30 min- pression (in patients complaining of mild to utes three times a week for 12 weeks, and moderate depression) to a greater degree they were compared with matched women than traditional psychotherapy. Additional participating in discussion groups and a advantages noted by the authors included nonintervention control group. The only less expense, no need to use antidepressant noted apparent benefit of exercise was a de- medication, and the persistence of a depres- crease in intake of stimulants (e.g., coffee) sion-free state when evaluated 12 months among exercisers, whereas there was an in- later, whereas half the patients receiving crease in intake among the nonexercisers.80 psychotherapy returned earlier for addi- These results are similar to the report of tional treatment. The reader is referredto an Penny and Rust,130 whose subjects partici- excellent review by Dunn and Dishman126 of pated in a walk-jog program involving \\% the relationship between exercise and de- miles of exercise twice a week for 15 weeks. pression. A comparison of personality scales mea- sured by the MMPI showed no difference One of the most distressing symptoms ex- from a control nonexercising group. Despite pressed by menopausal women is anxiety. these negative results, discussions with in- Vigorous physical activity reduces muscle dividuals who exercised elicited commonly tension and is also associated with a signif- observed responses: \"feeling better, enjoy- icant decrease in anxiety.127 This effect was ing social functions more, participating in noted only when the exercise was intense more extracurricular activities, and not enough to provoke significant elevations in being tired at day's end.\"130 The operative plasma epinephrine and norepinephrine, factors appear to be the frequency, inten- however,128 and did not occur if light to mod- sity, and duration of exercise, and patience. erate exercise wasperformed. The last is most important,as the benefits of exercise rarely occur before 10 weeks of Another common problem associated training, the time when most individuals with the menopausal syndrome—insom- drop out of exercise programs. nia—may be positively influenced by exer- cise. Healthy subjects who engaged in static In summary, although the chemical basis exercise (e.g., contraction of a hand dyna- of the mood improvement induced by phys- mometer at 40% of maximallevel for 40 min- ical activity is not known, fairly strong evi- utes, separated by a 10-minute rest at mid- dence suggests that acute and chronic vig- session) 2 hours before bedtime were orous exercise is associated with an shown to have a significantly reduced time improvement in affective states, especially to onset of sleep relative to nonexercise anxiety and moderate depression. nights. The improvement in sleep was as- sociated with increased slow-wave sleep Psychomotor speed is one well-recog- and decreased movement time during sleep, nized behavior that is slowed by aging. This
208 Developmental Phases is especially true for response speed that oc- generalized rather than specific exercise. curs in reaction time, performance of tasks For example, the reactive speed of the fin- that require the coordination of two simul- gers is improved in runners, who primarily taneous movements, writingspeed, and sim- exercise their legs.132 It is not clear whether ple tasks such as tapping in place.131 The this exercise-induced improvement affects quicker the response, the higher the percep- central nervous system processing time, or tual speed score. Perceptual speed was eval- motor speed. As with the psychologic re- uated in healthy aging women as part of a sponse to exercise, CNS function (e.g., large study examiningage-related changes, short-term memory) that is not impaired in and a progressive decrease was noted with a particular individual cannot be expected both chronologic and biologic aging.63 As to be improved by exercise. With this caveat shown in Table 11-8, the perceptual speed in mind, it is fair to conclude that \"exercise score decreased from a mean score of 64.4 seems to be one way for people to achieve ± 2.1 in 40-year-old premenopausal women maximal plasticity in aging,approximating to 48.0 ± 2.6 in 68-year-old women (p < full vigor and consistency of performance 0.0001; r = —0.41). An interesting observa- until life's end.\"132 tion is the difference in the perceptual speed score between premenopausal and post- SUMMARY menopausal women aged 46 to 55. Although the premenopausal women were only a few \"Menopause,\" an often-misused term, is years younger, their mean perceptual speed actually the duration of a woman'sfinalmen- score was significantly higher than that of strual period. The 15 years leading up to and the postmenopausal group, whose score following this event are known more prop- was similar to the score of women 5 or more erly as the \"climacteric.\" years past their menopause. Women lose a small percentage of bone as Further analysis of these data revealed a natural phenomenon in the aging process. that, within the groups, physical fitness was However, the greater the bone mineral con- positively correlated with the perceptual tent at bone mass maturity, the more one speed score. The greater the degree of fit- can afford to lose. Thus, women should be ness, the more functionally competent the encouraged during, and even before, the individual.63 This raises the issue ofwhether early climacteric to accrue as much bone as exercise may prevent premature agingof the possible, through an appropriate calciumin- central nervous system and compensate for take and an osteogenic exercise program. possible alterations in the neurohormonal Likewise, such practices can be used to milieu of postmenopausal women.A number avoid excessive bone loss during the climac- of investigators have shown that people who teric. For women who have osteoporosis, a exercise consistently have a faster reaction regimen of walking may be the safest type of time, and that this difference is related to Table 11-8. CHANGES IN PERCEPTUAL SPEED SCORE ASSOCIATED WITH CHRONOLOGIC AND BIOLOGIC AGING IN WOMEN Premenopausal Postmenopausal Age range 35-45 46-55 46-55 56-65 66-75 Mean age (± SEM) 40.9 ± 0.5 48.7 ± 0.4 52.2 ± 0.4 59.3 ± 0.5 68.5 ± 0.5 N 30 29 30 29 27 Perceptual speed score 64.4 ± 2.1 61.1 ± 1.9 56.6 ± 1.8 55.3 ± 1.3 48.0 ± 2.6 (mean ± SEM) Source: From Notelovitz et al,63 with permission.
Menopause 209 exercise program. These women should 9. Health United States, US Dept of Health and avoid exercises that emphasize flexion of Human Services, DHHS Pub No (PHS) 85- the back. 1232,1984. The postmenopausal period has been as- 10. Cohn SH, Abesamis C, Yasumura S, et al: sociated with an increased plasma total cho- Comparative skeletal mass and radial bone lesterol level and an increased LDL level— mineral content in black and white women. both risk factors for atherosclerotic disease. Metabolism 26:171,1977. A regular, long-term exercise program pro- motes beneficial changes in lipoprotein cho- 11. Parfitt AM: The cellular basis of bone re- lesterol levels, aerobic fitness, exercise modeling: The quantum concept re-exam- time, and coronary heart disease risk. ined in light of recent advances in cell biology of bone. Calcif Tissue Int 36:337, Exercise also adds to a feeling of well- 1984. being and may counteract clinical depres- sion and anxiety experienced by some 12. Katz JL, Yoon HS, Lipson S, et al: The effects women in this stage of life. of remodeling on the elastic properties of bone. Calcif Tissue Int 36:531,1984. REFERENCES 1. Jaszman LJB: Epidemiology of the climac- 13. De Deuxchaisnes C, Nagant: The pathogen- teric syndrome. In Campbell S (ed): The esis and treatment of involutional osteopo- Management of the Menopause and Post- rosis. In Dixon AHJ, Russel RGG, and Stamp menopausal Years. University Book Press, TCB (eds): Osteoporosis: A Multidisciplin- Baltimore, 1976, p 11. ary Problem. The Royal Society of Medicine. 2. Notelovitz M: Climacteric medicine and sci- Academic Press, London, 1983, p 291. ence: A societal need. In Notelovitz M, and van Keep P (eds): The Climacteric in Per- 14. Drinkwater BL, Nilson K, Chestnut III C, et spective. MTP Press Ltd, Lancaster, En- al: Bone mineral content of amenorrheic gland, 1986, p 19. and eumenorrheic athletes. N Engl J Med 3. Cummings SR, Rubin SM, and Black D: The 311:277,1984. future of hip fractures in the United States: Numbers, costs, and potential effects of 15. Riggs BL, Wahner HW, Dunn WL, et al: Dif- postmenopausal estrogen. Clin Orthop ferential changes in bone mineral density of 252:163,1990. appendicular and axial skeleton with aging: 4. Lewinnek G, Kelsey J, White A, et al: Signifi- Relationship to spinal osteoporosis. J Clin cance and comparative analysis of the epi- Invest 67:328, 1981. demiology of hip fractures. Clin Orthop 152:35, 1980. 16. Editorial: Osteoporosis and activity. Lancet 5. Keene JS, and Anderson CA: Hip fractures in 2:1365, 1983. the elderly, discharge predictions with a functional rating scale. JAMA 248:564, 1982. 17. Whedon GC: Interrelation of physical activ- 6. NCHS. Advance report of final mortality sta- ity and nutrition on bone mass. In WhitePL, tistics, 1989. Hyattsville, Maryland: US De- and Mondeika T (eds): Diet and Exercise: partment of Health and Human Services, Synergism in Health Maintenance. Ameri- Public Health Service, CDC (Monthly vital can Medical Association, Chicago, 1982, p statistics report, vol. 40, no. 8, suppl. 2), 99. 1992. 7. Public Health Service. Healthy people 2000: 18. Basset CA, and Becker RO: Generation of National health promotion and disease pre- electric potentials by bone in response to vention objectives—full report, with com- mechanical stress. Science 137:1063,1962. mentary. Washington DC: US Department of Health and Human Services, Public Health 19. Jones HH, Priest JD, Hayes WC, et al: Hu- Service, DHHS publication no. (PHS)91- meral hypertrophy in response to exercise. 50212, 1991. J Bone Joint Surg59A:204,1977. 8. Council on Scientific Affairs: Exercise pro- grams for the elderly. JAMA 252:544, 1984. 20. Orwoll ES, Ferar J, Oviatt SK, et al: The re- lationship of swimming exercise to bone mass in men and women. Arch Intern Med 149:2197, 1989. 21. Carter DR: Mechanical loading histories of bone remodelling. Calcif Tissue Int 36:S19, 1984. 22. Lanyon LE: Functional strain as a determi- nant for bone remodelling. Calcif Tissue Int 36:S56,1984. 23. Lanyon LE, and Rubin CT: Regulation of bone mass in response to physical activity. In Dixon AHJ, Russel RGG, and Stamp TCB (eds): Osteoporosis: A Multidisciplinary Problem. The Royal Society of Medicine. Ac- ademic Press, London, 1983, p 51.
210 Developmental Phases 24. Woo SLY,Kuei SC, Amiel D, et al: The effect 41. Rosenberg L, Hennekens CH, Rosner B, et of prolonged physical training on the prop- al: Early menopause and the risk of myocar- erties of long bone. J Bone Joint Surg dial infarction. Am J Obstet Gynecol 139:47, 63A:780, 1980. 1981. 25. Cavanaugh DJ, and Cann CE: Briskwalking 42. Szajderman B, and Oliver MF: Spontaneous does not stop bone loss in postmenopausal premature menopause, ischemic heart dis- women. Bone 9:201, 1988. ease and serum lipids. Lancet 1:962,1963. 26. Kirk S, Sharp CF, Elbaum N, et al: Effect of 43. Robinson RW, Higano N, and Cohen WD:In- long-distance running on bone mass in creased incidence of coronary heart disease women. J Bone Min Res 4:515,1989. in women castrated prior to menopause. Arch Intern Med 104:908,1959. 27. Kralner B, Toft B, Nielsen SP, et al: Physical exercise as prophylaxis against involutional 44. Bengtsson C, and Lindquist O: Menopausal vertebral bone loss: A controlled trial. Clin effects on risk factors for ischemic heart dis- Sci 64:541,1983. ease. Maturitas 1:165, 1979. 28. Brewer V, Meyer BM, Keele MJ, et al: Role of 45. Miller G, and Miller N: Plasma high density exercise in prevention of involutional bone lipoprotein concentration and development loss. Med Sci Sports Exerc 15:445,1983. of ischaemic heart disease. Lancet 1:16, 1975. 29. Linnell J, Stager JM, Blue PW, et al: Bone mineral content and menstrual regularity in 46. HaskellWL: The influence of exercise on the female runners. Med Sci Sports Exerc concentrations of triglyceride and choles- 16:343,1984. terol in human plasma. In Terjung RL (ed): Exercise and Sports Sciences Reviews. Col- 30. Marcus R, Cann C, Madvig P, et al: Menstrual lamore Press, Lexington, MA, 1984, p 205. function and bone mass in elite women dis- tance runners. Ann Intern Med 102:158, 47. Paffenbarger RS, Hyde RT, Wing AL, et al: A 1985. natural history of athleticism on cardiovas- cular health. JAMA 252:491,1984. 31. Myerson M, Gutin B, Warren MP, et al: Total body bone density in amenorrheic runners. 48. Salonen JT, Puska R, and Tuomilehto J: Obstet Gynecol 79:973,1992. Physical activity and risk of myocardial in- farction, cerebral stroke and death: A lon- 32. Rigotti NA, Nussbaum SR, Herzog DR, et al: gitudinal study in eastern Finland. Am J Ep- Osteoporosis in women with anorexia ner- idemiol 115:526,1982. vosa. N Engl J Med 311:1601, 1984. 49. Leon AS, Connett J, Jacobs DR, and Raura- 33. Notelovitz M, et al: Unpublished data. maa R: Leisure-time activity levels and risk 34. HeikkinenJ, Kurttila-Matero E, Kyllonen E, of coronary heart disease and death. The Multiple Risk Factor Intervention Trial. et al: Moderate exercise does not enhance JAMA 258:2388, 1987. the positive effect of estrogen on bone min- eral density in post-menopausal women. 50. Blair SH, Kohl HW III, Paffenbarger RS, et al: Calif Tissue Int (Suppl)49:S83,1991. Physical fitness and all-cause mortality: A 35. Notelovitz M, Martin D, Tesar R, et al: Estro- prospective study of health men and gen therapy and variable-resistance weight women. JAMA 262:2395, 1989. training increase bone mineral in surgically menopausal women. J Bone Min Res 6:583, 51. Castelli WP: Epidemiology of coronary heart 1991. disease. The Framingham Study. Am J Med 36. Chvapil M, Bartos D, and Bartos F: Effect of 76:4, 1984. long-term physical stress on collagen growth in the lung, heart and femur of young 52. Ducimetiere P, Eschwege E, Papoz L, et al: and adult rats. Gerontologia 19:263, 1973. Relationship of plasma insulin levels to the 37. Inkovaara J, Heikinheimo R, Jarvinen K, et incidence of myocardial infarction and cor- al: Prophylactic fluoride treatment and aged onary heart disease in a middle-aged popu- bones. Br Med J 3:73,1975. lation. Diabetologia 19:215, 1980. 38. Smith EL,Reddan W, and Smith PE: Physical activity and calcium modalities for bone 53. Manson JE, Rimm EB, Stampfer MJ, et al: mineral increase in aged women. Med Sci Physical activity and incidence of non-in- Sports Exerc 13:60,1981. sulin-dependent diabetes mellitus in 39. Sinaki M, and Mikkelsen BA: Postmeno- women. Lancet 338:774,1991. pausal spinal osteoporosis: Flexion versus extension exercises. Arch Phys Med Reha- 54. Manson JE, Nathan DM, Krolewski AS, et al: bil 65:593,1984. A prospective study of exercise and inci- 40. Goodman CE: Osteoporosis: Protective dence of diabetes among US male physi- measures of nutrition and exercise. Geriat- cians. JAMA 268:63, 1992. rics 40:59,1985. 55. Lapidus L, Bengtsson C, Larsson B, et al: Distribution of adipose tissue and risk of cardiovascular disease and death: A 12 year follow-up of participants in the population
Menopause 211 cholesterol and other plasma lipid and li- study of women in Gothenburg, Sweden. Br poprotein concentrations in middle-aged MedJ 289:1257,1984. male and female tennis players. Metabolism 56. Larsson B, Svardsudd K, Welin L, et al: Ab- 29:745,1980. dominal adipose tissue distribution, obe- 70. Harting GH, Moore CE, Mitchell R, et al: Re- sity, and risk of cardiovascular disease and lationship of menopausal status and exer- death: 13 year follow-up of participants in cise level to HDLcholesterol in women. Exp the study of men born in 1913. Br Med J Aging Res 10:13,1984. 288:1401, 1984. 71. Drinkwater B, Horvath S, and Wells C:Aer- 57. HaskellWL,and Superko R: Designingan ex- obic power of females ages 10 to 68. J Ger- ercise plan for optimal health. Family and ontol 30:385,1975. Community Health, p 72, May 1984. 72. Plowman S, Drinkwater B, and Horvath S: 58. Kilbom A: Physical training in women. Age and aerobic power in women: A longi- Scand J Clin Lab Invest 28(Suppl 119):1, tudinal study. J Gerontol 34:512,1979. 1971. 73. Notelovitz M, Fields C, Caramelli K, et al: 59. Wood P, and Haskell W: The effect of exer- Cardiorespiratory fitness evaluation in cli- cise on plasma high-density lipoproteins. macteric women: Comparison of two meth- Lipids 14:417,1979. ods. AmJ Obstet Gynecol 154:1009,1986. 60. Goffman J, Young W, and Tandy R:Ischemic 74. DeVries HA: Exercise and the physiology of heart disease, atherosclerosis and longev- aging. In DeVries HA: Exercise and Health. ity. Circulation 34:679, 1966. American Academy of Physical Education 61. Jacobs I, Lithell H, and Karlson J: Dietary ef- Papers, No. 17. Human Kinetics Publishers, fects on glycogen and lipoprotein lipase ac- Champaign, IL, p 76,1984. tivity in skeletal muscle of men. Acta Physiol 75. Zauner C, Notelovitz M, Fields CD,et al: Car- Scand 115:85,1982. diorespiratory efficiency at submaximal 62. Lamon-Fava S, Fisher EC, Nelson ME, et al: work in young and middle-aged women. Am Effect of exercise and menstrual cycle status J Obstet Gynecol 150:712,1984. on plasma lipids, low density lipoprotein 76. Dehn MM, and Bruce RA:Longitudinal vari- particle size, and apolipoproteins. J Clin En- ations in maximum oxygen intake with age docrinol Metab 68:17,1989. and activity. J Appl Physiol 33:805,1972. 63. Notelovitz M, Dougherty M, Resnick J, et al: 77. jAstrand I: Aerobic work capacity in men The psychosocial and biologic adaptation to and women with special reference to age. aging in women. Final Report NIA #R01 Acta Physiol (Scand) 49:45,1960. AG00796-03,1982. 78. Cowan MM, and Gregory LW: Responses of 64. Busby J, Notelovitz M, Putney K, et al: Ex- pre- and postmenopausal femalesto aerobic ercise, high density lipoprotein cholesterol conditioning. Med Sci Sports Exerc 17:138, and cardiorespiratory function in climac- 1985. teric women. South Med J 78:769, 1985. 79. White MK, Venter RA, Martin RB, et al: Ef- 65. Franklin B, Buskirk E, Hodgson J, et al: Ef- fects of aerobic dancing and walkingon car- fects of physical conditioning on cardiore- diovascular function and muscular strength spiratory function, body composition and in postmenopausal women. J Sports Med serum lipids in relatively normal weight and 24:159, 1984. obese middle-aged women. Int J Obes 3:97, 80. Gill AA, Veigl VL, Shuster J, et al: A well- 1979. woman's health maintenance study com- 66. Rotkis T, Boyden TW, Pamenter RW, et al: paring physical fitness and group support High density lipoprotein cholesterol and programs. Occup Ther J Res 4:286, 1984. body composition of female runners. Me- 81. Notelovitz M, Fields C, Caramelli K, et al: Al- tabolism 30:994, 1981. ternatives to hormone therapy. Presented at 67. Notelovitz M, Feldman E, Larsen S, and Xlth World Congress of Obstetrics and Gy- Khan F: Lipids and lipoproteins in post- necology, October 1985. menopausal women: Effect of route of estro- 82. Probart CK, Notelovitz M, Martin D, et al: gen administration and aerobic exercise. In The effect of moderate aerobic exercise on Christiansen C, and Overgard K (eds): Os- physical fitness among women 70years and teoporosis. Third International Symposium older. Maturitas 14:49, 1991. on Osteoporosis, Copenhagen, Denmark, 83. Profant GR, Early RG, Nilson KL, et al: Re- October 1990, p 1822. sponse to maximal exercise in healthy mid- 68. Moore CE, Hartung GH, Mitchell RE, et al: dle-aged women. J Appl Physiol 33:595, The effect of exercise and diet on high-den- 1972. sity lipoprotein cholesterol levels in 84. Bruce RA, DeRouen TA, and Hossack KF: women. Metabolism 32:189,1983. Pilot study examining the motivational ef- 69. Vodak PA,Wood PD, Haskell WL, et al: HDL-
212 Developmental Phases fects of maximal exercise testing to modify 100. HurleyBF, Seals AA, EhsaniAA,et al: Effects risk factors and health habits. Cardiology of high-intensity strength training on car- 66:111,1980. diovascular function. Med Sci Sports Exerc 85. Glassford RG, Baycroft GHY, SedgwickAW, 16:483,1984. et al: Comparison of maximaloxygen uptake values determined by predicted and actual 101. Hammar M, Berg G, and Lindgren R: Does methods. J Appl Physiol 20:509,1965. physical exercise influence the frequency of 86. Cink RE, and Thomas TR: Validity of the As- postmenopausal flushes? Acta Obstet Gy- trand-Rhyming monogram for predicting necol Scand 69:409, 1990. maximal oxygen uptake. Br J Sports Med 15:182,1981. 102. Tataryn IV,Lomax P, Meldrum DR,et al: Ob- 87. Shoenfeld Y, Keven G, ShimoniI, et al: Walk- jective techniques for the assessment of ing. A method for rapid improvement of postmenopausal hot flashes. Obstet Gyne- physical fitness. JAMA 243:2062,1980. col 57:340,1981. 88. Caramelli KE, and Notelovitz M: Effect of load-bearing during treadmill walking in 103. Schiff I, Tulchinsky D, Cramer D, et al: Oral women aged 57 to 67 years (abstr). Maturi- medroxyprogesterone in the treatment tas 6:95, 1984. of postmenopausal symptoms. JAMA 89. Zadik Z, Chalew SA, McCarter RJ, et al: The 244:1443, 1980. influence of age on the 24-hour integrated concentration of growth in normal individ- 104. Erlik Y, Meldrum DR, Lagasse LD, et al: Ef- uals. J Clin Endocrinol Metab 60:513,1985. fect of megestrol acetate on flushing and 90. Lang I, Schernthaner G, Pietschmann P, et bone metabolism in post-menopausal al: Effects of sex and age on growth hormone women. Maturitas3:167,1981. response to growth hormone-releasing hor- mone in healthy individuals.J Clin Endocri- 105. Lanska DJ, Lanska MJ, Hartz AJ, and Rimm nol Metab 65:535,1987. AA: Factors influencing anatomic locationof 91. Grimby G, and Saltin B: The aging muscle. fat tissue in women. Int J Obes 9:29,1985. Clin Physiol 3:209,1983. 92. Rudman D, Feller AG, Nagraj HS, et al: Ef- 106. Shimokata H, Tobin JD, Muller DC, et al: fects of growth hormone in men over 60 Studies in the distribution of body fat: I. Ef- years old. N Engl J Med 323:1,1990. fects of age, sex and obesity. J Gerontol 93. Fisher MB,and Birren JE: Age and strength. 44:M66, 1989. J Appl Psychol 31:490,1947. 94. Montoye HJ, and Lamphiear DE: Grip and 107. Eckel RH: Lipoprotein lipase. A multifunc- arm strength in males and females age 10- tional enzyme relevant to common meta- 69. Res Q 48:109,1977. bolic diseases. N Engl J Med 320:1060, 95. Tzanoff SP, and Norris AH: Effect of muscle 1989. mass decrease on age-related BMR changes. J Appl Physiol 43:1001,1973. 108. Rebuffe-Scrive M, Eldh J, Hafstrom L-O, and 96. Joman VR, Veikko AK, Deibert D, et al: In- Bjorntorp P: Metabolism of mammary, ab- creased insulin sensitivity and insulin bind- dominal, and femoral adipocytes in women ing to monocytes after physical training.N before and after menopause. Metabolism Engl J Med 301:200, 1979. 35:792, 1986. 96a. Van Dam S, Gillespy M, Notelovitz M, and Martin AD:Effect of exercise on glucose me- 109. Rebuffe-Scrive M, LonnrothP, Marin P, et al: tabolism in postmenopausal women. Am J Regional adipose tissue metabolism in men Obstet Gynecol 159:82, 1988. and postmenopausal women. Int J Obes 97. Wells JB, Jokl E, and Bohanen J: The effect 11:347,1987. of intensive physical training upon body composition of adolescent girls. J Assoc 110. Rebuffe-Scrive M, Basdevant A, and Guy- Phys Mental Rehab 17:68,1963. Grand B: Effect of local application of pro- 98. Brown CH, and Wilmore JH: The effects of gesterone on humanadipose tissue lipopro- maximal resistance training on strength and tein lipase. Horm Metab Res 15:566,1983. body composition of women athletes. Med Sci Sports Exerc 6:174, 1974. 111. Rebuffe-Scrive M: Steroid hormones and 99. Wilmore JH: Alterations in strength, body distribution of adipose tissue. Acta Med composition and anthropometric measure- Scand (Suppl)723:143,1988. ments consequent to a 10-weekweight train- ing program. Med Sci Sports 6:133, 1974. 112. Despres JP, Bouchard C, Savard R, et al: The effect of a 20-week endurance training pro- gram on adipose tissue morphology and li- polysis in men and women. Metabolism 33:235,1984. 113. Tremblay A, Despres JP, Leblanc C, and Bouchard C: Sex dimorphism in fat loss in response to exercise-training. J Obes Weight Regul 3:193, 1984. 114. Tremblay A, Despres JP, and Bouchard C: Alteration in body fat and fat distribution during growth and later health conse- quences. In Bouchard C, and Johnston FE:
Menopause 213 Current Topics in Nutritionand Disease, Vol 124. Levin DC: The runner's high: Fact or fiction? 17. Alan R Liss, New York, 1988. JAMA 248:24,1982. 115. Despres JP, Tremblay A, Nadeau A, and Bouchard C: Physical training and changes 125. Greist JH, Klein MH,Eicchens RR,et al:Run- in regional adipose tissue distribution. Acta ning as treatment for depression. Comp Psy- Med Scand (Suppl)723:205,1988. chiatry 20:41,1979. 116. Bullough PG:Pathologic changes associated with the common arthritides and their treat- 126. Dunn AL, and Dishman RK: Exercise and the ment. Pathol Annu 14:69,1979. neurobiology of depression. Exerc Sport Sci 117. Gordon T: Osteoarthritis in U.S. adults. In Rev 19:41,1991. Bennett BH, and Wood PHN (eds): Popula- tion Studies in the Rheumatic Diseases. Ex- 127. Morgan WP: Anxiety reduction following cerpta Medica, New York, 1968, p 391. acute physical activity. Psychiatr Annu 9:36, 118. Brincat M, Moniz CT, Studd JWW, et al: Skin 1979. thickness and skin collagen mimic an index of osteoporosis in the postmenopausal 128. Morgan WP, Horstman DH, Cymerman A, et woman. In Christiansen C, Arnaud CD,Nor- al: Facilitation of physical performance by din BEC, et al (eds): Osteoporosis. Copen- means of cognitive strategy. Cog Ther Res hagen International Symposium on Osteo- 7:251,1983. porosis, June 3-8,1984, p 353. 119. Vandenbroucke JP, Witteman JC, Valken- 129. Browman CP: Sleep following sustained ex- burg HA, et al: Noncontraceptive hormones ercise. Psychophysiology 17:577,1980. and rheumatoid arthritis in perimeno- pausal and postmenopausal women. JAMA 130. Penny GD,and Rust JO: Effect of a walking- 255:1299, 1986. jogging program on personality character- 120. Lane NE, Bloch DA, Jones HH, et al: Long- istics of middle-aged females. J Sports Med distance running, bone density and osteo- 20:221,1980. arthritis. JAMA 255:1147, 1986. 121. Panush RS, Schmidt C, Caldwell JR, et al: Is 131. Spirduso WW:Exercise as a factor in aging running associated with degenerative joint motor behavior plasticity in exercise and disease? JAMA 255:1152,1986. health. American Academy of Physical Ed- 122. Weber JC, and Lee RA: Effects of differing ucation Papers, No. 17. Human Kinetics pre-puberty exercise programs on the emo- Publishers, Champaign, IL, 1984, p 89. tionality of male albino rats. Res Q 39:748, 1968. 132. Spirduso WW, and Clifford P: Replication of 123. Olson EB Jr, and Morgan WP: Rat brain age and physical activity effects in reaction monoamine levels related to behavioral as- and movement time. J Gerontol 33:26, 1978. sessment. Life Sci 30:2095,1982. 133. Adams G, and DeVries H: Physiological ef- fects of an exercise training regimen upon women aged 52 to 79. J Gerontol 28:50,1973. 134. Sidney K, Shephard R, and Harrison J: En- durance training and body composition of the elderly. Am J Clin Nutr 30:326,1977. 135. Sidney K, and Shephard R: Frequency and intensity of exercise training for elderly subjects. Med Sci Sports Exerc 10:125,1978.
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Ill Special Issues and Concerns
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12CHAPTER The Breast CHRISTINE E. HAYCOCK, M.D. BREAST SUPPORT PREGNANCY AND LACTATION NIPPLE INJURY PREMENSTRUAL CHANGES AND TRAUMA FIBROCYSTIC BREASTS BREAST AUGMENTATION AND EXERCISE FOLLOWING TRAUMA REDUCTION OR SURGERY w saring a bra can provide two useful functions duringexercise—providing support and limiting breast motion.1,2 This can help reduce discomfort and impact of the breast against the anterior chest wall. Paddingcan be added to help prevent traumatic injuries, such as that from a hockey stick or an elbow. There is no evidence that free-swinging breasts are more likely to be dam- aged during exercise. However, women in primitive cultures who never wear bras do develop long pendulous breasts, whereas those in modern society who frequently wear bras are less likely to develop these changes. BREAST SUPPORT In an effort to ascertain the injury potential for the female athlete in the early 1970s, two surveys were conducted in more than 300 physical education depart- ments throughout the country. The first questionnaire, performed by JoanGil- lette, A.T.C., and published in 1975 in The Physician and Sportsmedicine,3 asked for the numbers and types of injuries seen by coaches and trainers. I sent out a more detailed questionnaire to cover the 1974to 1975season, with more empha- sis on the types of injuries rather than on just the numbersand associated sports. The combined results of the two surveys were published in 1976.4 The surveys indicated that, in general, the types and numbers of injuries to these female ath- letes were essentially the same as to their male counterparts. Of particular inter- est to me was the fact that, of all injuries reported, those to the breast were least common. Other studies have confirmed these findings.5-7 217
218 Special Issues and Concerns The results of the earlier surveys Twelve female athletes with different breast prompted me to undertake a third survey,8 sizes were fitted with special supportive specifically asking if female athletes re- bras. They were encouraged to use these ported tenderness or soreness in their garments during athletic competition and to breasts or injuries such as scratches from note how they compared in comfort and metallic parts or allergies to the materialsin support with the bras they had been using their bras. Thirty-onepercent of the respon- previously. Most of the women felt that the dents indicated sore or tender breasts after bulky test bras provided better support than exercise. Of these, 52% reported specific their own. The women who benefited the minor injuries to the breasts. most had size B cups or larger. Fivevolun- teers were filmed with a high-speed (100 A study was undertaken by Haycock, frames per minute), 16-mm camera while Shierman, and Gillette9 to ascertain what walking and running on a treadmill and factors cause breast injury and discomfort. while jumping to simulate the motion of To determine if a bra is necessary to control shooting a basketball into the hoop. A breast motion, a test was instituted to mea- marker was placed on each nipple so that sure breast movement during exercise. line studies made by tracing each frame could be drawn. Each markerwas placed ei- Figure 12-1. The subject wore a size D cup. The solid ther on the bra or on the breast itself, since line represents the range of motion with no bra; the the athletes were filmed wearing their own dash-dot-dash line, the subject's own bra, which had bras, wearingthe special bras or wearingno fairly good support; and the dash line, the speciallyfit- bras. ted bra, showing the best support. The films showed that during running, the breast moves considerably up and down, and duringjumping, the breasts roll in a spi- ral motion (Fig. 12-1). Although the force of breast impact upon the chest wall was not measured, it was estimated to be between 60 and 80 foot pounds per square inch, with the largest breasts exerting the greatest force. Although both sets of bras limited motion, the specially fitted ones did the best job, corroborating the increased support and comfort reported by the athletes them- selves. These findings are consistent with the original expectations of the authors. The natural support of the breasts is minimal. The breast is composed mostly of adipose tissue. It is held in place by the skin and some deep fascial structures, which loosely attach the glands to the underlying muscles, blood vessels, and nerves. Cooper's liga- ments do not support the breasts. They are merely connective tissue strands extending between the skin and the pectoralis fascia and separating the glandular structures.8As a result of this study, the following recom- mendations regarding sports bras can be made:9
The Breast 219 1 A bra should be made of firm, mostly ples and cause soreness and sensitivity to nonelastic material with good absorp- touch and temperature change. The use of tive qualities (about 60% cotton plus windbreaking material over the chest area about 40% synthetic materials for fast helps prevent this type of injury. There is no drying and easy laundering). More elas- treatment for cold injury to nipples, except ticity provides less support. for supportive measures. Athletes should be cautioned to prevent such injury by avoid- 2 It should be constructed to limit motion ing cold exposure.21,22 in all directions and providefirmsup- port. There should be either no seams TRAUMA over the nipples or smooth seams that will not irritate. Blows to the breasts by field hockey sticks, pucks, elbows, kicks, and other ob- 3 Some provision should exist for inser- jects certainly occur but seldom result in tion of padding, if indicated to reduce more than mild contusions. This superficial the risk of traumatic injury. Obviously, capillary damage may look significant but a bra intended only for use during run- usually responds well to the simple appli- ning does not need these features. cation of cold for 10 to 20 minutes. Edema and ecchymosis gradually resolve within 4 All metal or plastic hooks or catches weeks. should be well covered to protect the wearer from skin irritation or abra- A severe blow to the breast may cause a sion.8,10,11 Various types of bras have hematoma owing to subcutaneous bleeding been studied.12-16 In the most recent from deeper vessels. Hemostasis usually is study, Dr. Deana Lorentzen of Utah attained spontaneously, and most breast he- State University at Logan17 compared matomas resolve spontaneously too. A eight of the most popular bras currently breast hematoma should be evacuated only on the market. Her findings were in if accompanied by increasing pain, increas- agreement with the previous recom- ing size, or possible infection. If a fibrous mendations. Dr. Lorentzen alsosug- nodule remains after resolution or evacua- gested adding an underwire. Many ath- tion of a hematoma, its removal may be nec- letes prefer this type of bra, as do many essary. larger-breasted women, regardless of their exercise habits. There is no evidence that trauma to the breast causes cancer.23-25 However, breast NIPPLE INJURY injury usually leads to careful examination, and previously undetected masses are more \"Runners' nipples\" is a condition in likely to be appreciated as a result of more which the nipples are irritated, abraded, careful scrutiny. and/or lacerated18-20 by the rubbingofcloth- ing on the nipple during activity over a BREAST AUGMENTATION AND prolonged period of time. Any type ofrough- REDUCTION surfaced cloth or seam can cause this prob- lem. Male runners can wear Band-Aids over Cosmetic surgery involving eitheraug- their nipples to prevent this from happening mentation or reduction of the breast can to them. Female runners can wear well-de- cause special problems. Following breast signed bras to protect their nipples. An augmentation, a swimmer was unable to abrasion of the nipple can lead to infection. swim at her previous freestyle speed despite regaining all her previous skills and Exposure to cold can damage the nipples, strength and regaining her previous back- too. A combination of moisture from perspi- ration with evaporation and wind chill can lower nipple temperature to injure the nip-
220 Special Issues and Concerns stroke speed. Her larger breasts increased transient increases in the concentration of her resistance against the water. She was lactic acid in breast milk following maximal able to accept this loss of speed because she exercise, but it is not known whether this al- felt an increase in her breast size from 32A teration is of any significance. Lovelady, to 34Bmore than compensated psychologi- Lonnerdal, and Dewey31 demonstrated no cally. However, a more competitive swim- differences in milk composition between ex- mer probably would not have been content ercising and sedentary lactating women. to sacrifice speed for the emotional benefit The exercising women in this study tended of a more personally satisfying appear- to have greater milk energy and volume, but ance.26 Dr. K. Barthels of California showed the differences were not statistically signifi- that simulated augmentation of the breasts cant, possibly because of the small numbers slowed swimmers with specific heights and of subjects studied (n = 8 in each group). weights but did not slow others.27 PREMENSTRUAL CHANGES Athletes in contact sports probably AND FIBROCYSTIC BREASTS should not undergo breast augmentation. Blunt chest trauma can cause rupture of the Many female athletes experience breast prosthesis, with resultant hemorrhage and discomfort premenstrually. This may be re- deformity of the breasts.28 duced by wearing a supportive bra and by taking bromocriptine or danazol orally, if in- There are no studies to show whether a dicated. Premenstrual mastalgia may also reduction in breast size improves swim occur in women who have fibrocystic speed in large-breasted swimmers, but this changes. About 50% of women have some possibility has been suggested.27 Theoreti- clinical evidence of this process. No specific cally, breast reduction might improve the therapy has proved effective, although some performance of large-breasted athletes, par- investigators have advocated a reduction of ticularly those in nonaquatic endurance methylxanthine consumption or adminis- sports. Several top track coaches feel that tration of vitamin E or of danazol.32-34 (See large-breasted women do not perform as Chapter 13for additional discussion.) A sup- well as small-breasted women in running portive bra is helpful for these women, too. events. This impression remains anecdotal In addition to wearing it during exercise, and unconfirmed and, if real, may relate to athletes with nocturnal discomfort mayfind carrying less fat weight as well as having al- it helpful to wear it while sleeping as well. tered contours and resistance factors. Any breast masses should be evaluated PREGNANCY AND LACTATION with mammography and probably also so- nography. Diagnostic needle aspiration of Physiologic breast enlargement during breast cysts may be therapeutic. If a cyst re- pregnancy has not been shown to hinder solves completely following aspiration, bi- athletic performance, which usually de- opsy is not necessary. Persistence of a cyst clines during pregnancy, particularly for following attempted needle aspiration re- sports requiring speed. It is impossible to quires excisional biopsy for diagnosis. isolate the effects of breast enlargement, ab- dominal enlargement, weight gain, altered All athletes should practice monthly center of gravity, and hormonal changes in breast self-examination. This is bestper- determining causal relationships. A good formed at the end of menses, when palpable supporting bra is certainly useful to the physiologic changes from hormonal influ- pregnant exerciser.29 ence are minimal. The American CancerSo- ciety, the American College of Radiology, Several studies of the effects of exercise the American Medical Association, the Col- upon lactation have shown no adverse ef- lege of American Pathologists, and the Na- fects. Wallace and Rabin30 have reported
The Breast 221 tional Cancer Institute have endorsed the women's varsity athletic program. Phys following guidelines for screening mam- Sportsmed 6(3):112,1978. mography: 7. Zelisko JA, Noble B, and Porter M:A compar- ison of men's and women's professional bas- 1 Onset or baseline mammography by ketball injuries. Am J Sports Med 10:297, age 40 1982. 8. Haycock C: A need to know: Joggers' breast 2 Mammography every 1 to 2 years be- pain. Response. Phys Sportsmed 7(8):27, tween ages 40 and 49 1979. 9. Haycock C, Shierman G, and Gillette J: The fe- 3 Annual mammographythereafter.35 male athlete—does her anatomy pose prob- lems? Proceedings of the 19th Conference on EXERCISE FOLLOWING the MedicalAspects of Sports, AMA, 1978. TRAUMA OR SURGERY 10. Haycock CE: Breast support and protection in the female athlete. AAHPER Research Con- Appendix A discusses the appropriate re- sortium Symposium Papers 1:50,1978. turn to exercise following various types of 11. Report: Female athletes need good bras, MD breast surgery, as well as trauma. reports. Phys Sportsmed 5(8): 15, 1977. 12. Baynes JD: Pro+ Tec Protective Bra. J Sports SUMMARY Med Phys Fitness 8:34,1968. 13. Hunter L: The bra controversy: Are sports Breast problems in the female athlete can bras a necessity? Phys Sportsmed 10(11):75, at times be of serious import to the partici- 1982. pant, but usually they fall more into the cat- 14. Gehlsen G, and Albohm M: Evaluation of egory of a nuisance to performance, when sports bras. Phys Sportsmed 8(10):89,1980. size and resultant discomfort are a factor. 15. Schuster K: Equipmentupdate: Jogging bras Trauma and tumors are responsible for the hit the streets. Phys Sportsmed 7(4): 125, more disturbing conditions. 1979. 16. Survey: Women marathoners describe bra The use of good supporting bras for the needs. Phys Sportsmed 5(12):12, 1977. large-breasted athlete is certainly indicated 17. Lorentzen D, and Lawson L: Selected sports and can make athletic events more enjoya- bras: A biomechanical analysis of breast ble for these individuals. Cosmetic surgery motion while jogging. Phys Sportsmed is best relegated to the postathletic phase of 15(5):128,1987. life. 18. Levit F: Jogger's nipples. N Engl J Med 297:1127,1977. REFERENCES 19. Cohen HJ: Jogger's petechiae. N Engl J Med 279:109, 1968. 1. Haycock C: Supportive bras for jogging. Med 20. Corrigan AB, and Fitch KD:Complications of Aspects Hum Sexuality. 14:6,1980. jogging. Med J Aust2:363,1972. 21. Powell B: Bicyclist's nipples. JAMA 249:2457, 2. Haycock C: The female athlete and sports- 1983. medicine in the 70's. J Florida M A 67:411, 22. Adrian MJ: Proper clothing and equipment. 1980. In Haycock CE (ed): Sports Medicine for the Athletic Female. Medical Economics Book 3. Gillette J: When and where women are in- Div, Oradell, NJ, 1980, p 61. jured in sports. Phys Sportsmed 3(5):61, 23. Karon SE:Medical testimony in a trauma and 1975. breast cancer case, showing the direct and cross-examinations of the plaintiff's internist 4. Haycock C, and Gillette J: Susceptibility of and the defendant pathologist. Med Trial women athletes to injury: Myths vs reality. Tech Q 13:361,1967. JAMA 236:163, 1976. 24. Stevens M: Traumatic breast cancer. Med Trial Tech Q 25:1,1978. 5. Whiteside PA:Men's and women's injuries in 25. Dziob JS: Trauma and breast cancer, or the comparable sports. Phys Sportsmed anatomy of an insurance claim. RI Med J 8(3):130, 1980. 63:37, 1980. 26. Levine NS, and Buchanan RT: Decreased 6. Eisenberg I, and Allen WC: Injuries in a swimming speed following augmentation mammoplasty. Plast Reconstr Surg 71:255, 1983.
222 Special Issues and Concerns 27. Barthels KM: Discussion—decreased swim- 32. Minton JP, Abou-Isaa H, Reiches N, et al: Clin- ming speed following augmentation mam- ical and biochemical studies on methyl-xan- moplasty. Plast Reconstr Surg 71:257,1983. thine related fibrocystic breast disease. Sur- gery 90:301, 1981. 28. Dellon AL: Blunt chest trauma: Evaluationof the augmented breast. J Trauma 20:982,1980. 33. Ernster VL, Mason L, Goodson WH, et al: Ef- fects of caffeine-free diet on benign breast 29. Shangold M: Gynecological and endocrine- disease: A randomized trial. Surgery 91:263, logical factors. In Haycock C (ed): Sports 1982. Medicine and the Athletic Female. Medical Economics Book, Oradell, NJ, 1980. 34. London RS, Sundaram GS, Schultz M, et al: Endocrine parameters and alpha-tocopherol 30. Wallace JP, and Rabin J: The concentration of therapy of patients with mammary dysplasia. lactic acid in breast milk following maximal Cancer Res 41:3811,1981. exercise. Int J Sports Med 12:328, 1991. 35. Mammography screening urged: Major med- 31. Lovelady CA, Lonnerdal B, and Dewey KG: ical groups agree on guidelines. ACR Bull Lactation performance of exercising women. 45:1, 1989. Am J C l i n N u t r 52:103,1990.
13CHAPTER Gynecologic Concerns in Exercise and Training MONA M. SHANGOLD,M.D. CONTRACEPTION PREMENSTRUAL SYNDROME Oral Contraceptives Intrauterine Devices (lUDs) FERTILITY Mechanical (Barrier) Methods Norplant STRESS URINARY INCONTINENCE Choosing a Contraceptive POSTOPERATIVE TRAINING AND DYSMENORRHEA RECOVERY ENDOMETRIOSIS EFFECT OF MENSTRUAL CYCLE ON PERFORMANCE A iletic women have many concerns about the effects of regular training upon various gynecologic conditions, the effects of various gynecologic conditions and their treatments upon exercise performance, and the effects of endogenous and exogenous hormones upon exercise and health parameters. Menstrual and hormonal changes associated with exercise and training are discussed compre- hensively in Chapter 9. This chapter will address what is known about other gynecologic concerns of the athlete, including contraception, dysmenorrhea, premenstrual syndrome, fertility, stress urinary incontinence, and cyclic changes in exercise performance. CONTRACEPTION Although oral contraceptives have been reported to be the most popular form of contraception among American women,1 two surveys have found that runners prefer diaphragm use.2,3 In a survey of the 1841 women who entered the 1979 New York City Marathon, Shangold and Levine2 reported that 37%of the 394 respondents were diaphragm users, while only 6% were oral contraceptive users. Jarrett and Spellacy3 surveyed runners through a newspaper advertisement and found that 44%of the 70 respondents used diaphragms, while only 13% used oral contraceptives. Thus, based on these survey data, it seems that at the timeof these studies runners preferred the diaphragm over any other form of contraception. 223
224 Special Issues and Concerns Oral Contraceptives tent advantages over the standard (mono- phasic) pills containing 30 to 35 ug of estro- Many women are concerned about side ef- gen and seem to lead to more breakthrough fects and complications associated with oral bleeding and confusion. contraceptive use, and such fears have un- Because of the beneficial effects of endur- doubtedly limited the use of these agents. ance training upon some parameters af- However, most of the reported and publi- fected adversely by oral contraceptives cized side effects and complications were (e.g., coagulation, lipid metabolism, and associated with higher-dose pills than are carbohydrate metabolism), several investi- generally prescribed now. Studies have gators have studied the combined effects of shown that the low-dose pills, each contain- exercise and oral contraceptives on these ing 30 to 35 ug of ethinyl estradiol, are much variables. safer than the pills containing 50 or more /ug Oral contraceptives are associated with a of ethinyl estradiol, offering reductions in number of changes in coagulation and fibri- cardiovascular and thromboembolic risks. nolytic factors in both sedentary and trained Many of the adverse effects of oral contra- women. Plasma plasminogen activator, ceptives on thrombosis, arterial disease, which converts plasminogen to plasmin, is and lipid and carbohydrate metabolism are increased by oral contraceptive use and is related to the progestin content of the further increased by exercise.10 Huisveld pill.4-8 As described in an excellent review and co-workers11 reported that oral contra- article by Mishell,9 despite the detrimental ceptive users have increased total plasmin- effects associated with steroid contracep- ogen and free plasminogenlevels, increased tives, women who take these agents actually factor XII and decreased Cl-inactivator and have a reduced incidence of heavy bleeding, increased factor XH-dependentfibrinolytic irregular bleeding, endometrial cancer, sev- activity, higher activity levels of normal eu- eral types of benign breast disease, ovarian globulin fraction-fibrinolytic activity and ex- carcinoma, rheumatoid arthritis, and salpin- trinsic (tissue-type) plasminogen activator, gitis, compared with womenwho do not take and decreased urokinase-like fibrinolytic oral contraceptives. activator activity. Hedlin, Milojevic, and Low-dose oral contraceptive agents were Korey12 confirmed the increased fibrinolytic first introduced in 1973 and have grown in activity induced by exercise or oral contra- availability since then. They are probably ceptive use or both, and they have also used more widelynow than at the time of the shown that exercise raises antithrombin III surveys cited. Progestin-onlypills were first activity, whereas oral contraceptive use marketed in 1973 and were intended for lowers it. In this study, the hemostatic those women for whom estrogen is contra- change induced by oral contraceptives was indicated; these pills have a high incidence offset by exercise. It is probable that exer- of breakthrough bleeding, and their use is cise and training offset any net tendency to- rarely indicated. Oral contraceptive agents ward increased coagulability induced by containing less than 30 /ugof estrogen also oral contraceptive use. have a high incidence of breakthrough Powell and colleagues13 demonstrated bleeding and are poorly tolerated by most that several different oral contraceptive women as a result. Biphasic preparations agents alter lipoprotein lipid levels ad- were first introduced in 1982 and werefol- versely, raising total triglyceride,total cho- lowed by the introduction of triphasic prep- lesterol, and low-density lipoprotein (LDL) arations in 1984. In these pills, the doses of cholesterol significantly. However, the re- progestin, and occasionally of estrogen, are port by Gray, Harding, and Dale14 showed different on different days. These newest that runners taking oral contraceptives have agents have not been proved to offer consis- lipid profiles similar to those of runnerstak-
Gynecologic Concerns in Exercise and Training 225 ing no hormonal medication, suggesting has never had a pelvic infection, prpvided that exercise may offset the adverse effects that menorrhagia and/or dysmenorrhea do of oral contraceptive agents upon lipidlev- not ensue and impair the athletic perfor- els. mance. In view of the many beneficial effects Mechanical (Barrier) Methods known about oral contraceptive use, it re- Mechanical methods of contraception are mains unclear why these agents are not cho- sen by more female athletes. It is likely that acceptable for all women who are motivated many avoid using them because of un- and reliable enough to use them.Dia- founded fears based on reported side effects phragms and condoms are more effective of the higher-dose oral contraceptive agents when used in combination with contracep- (containing 50 ng or more of estrogen). tive foam or jelly. The sponge is no more ef- However, the weight gain, bloating, depres- fective than the diaphragm and has been re- sion, and mood changes associated with ported to be associated with more local higher dosages are uncommon with pills irritation and other side effects. The main containing less than 50 ug of estrogen. The disadvantages of mechanical (barrier) two major side effects associated with use of methods of contraception are their messi- the lower-dose agents are breakthrough ness, inconvenience, and disruption of sex- bleeding (i.e., bleeding on the days of hor- ual activity. Since athletes tend to be moti- mone ingestion) and amenorrhea (i.e., lack vated and disciplined, these deterrents are of withdrawal bleeding at the end of each usually considered minor. However, leakage hormone cycle). Each of these is a nuisance of vaginal contraceptive jelliesor foams dur- but not of serious consequence. Break- ing exercise may be uncomfortable.When through bleeding may resolve spontane- added to vaginal secretions and semen, the ously within three cycles; if it does not, it volume of such discharge may be substan- may resolve with additional hormone ther- tial and annoying during exercise. This apy, either transiently or permanently. problem may be remedied by placing a sec- Amenorrhea rarely resolves spontaneously ond, smaller diaphragm distal to the first, by but usually resolves with short-term or long- inserting a vaginal tampon, or, preferably, term ingestion of additional estrogen or less by wearing a minipad. progestin. Diaphragm use requires vaginal retention Intrauterine Devices of the diaphragm for 6 to 8 hours following Intrauterine contraceptive devices (lUDs) the last vaginal ejaculation. Some athletes may find it uncomfortable to exercise with a were associated with an increased preva- diaphragm in the vagina; such women may lence of menorrhagia (heavy menstrual benefit from refitting with a slightlysmaller bleeding) and dysmenorrhea (painful men- diaphragm, which will provide equal contra- struation), each of which could impair ath- ceptive efficacy and greater comfort. letic performance. Only two lUDs currently are available in the United States: ParaGard, Norplant which contains copper, and Progestasert, Norplant is a subdermal implant system which contains progesterone. Manufacture of all other lUDs that previously were avail- that recently has been approved for long- able has been discontinued for economic term contraception.15 It is made up of six reasons, primarily expensive litigation slender capsules containing levonorgestrel, (mostly unwarranted). An IUDis an accept- which are implanted in the upper arm. The able contraceptive choice for the athlete levonorgestrel in each capsule is released who is in a monogamous relationship and slowly, providing contraception for about 5
226 Special Issues and Concerns years. The primary mechanism of action is style. Women who have coitus once weekly suppression of ovulation, and the major side or less frequently probably should use bar- effects are irregular bleeding and head- rier methods of contraception, unless there aches. The major advantages of this subder- is an additional reason to use oral contra- mal implant are its long effectiveness, com- ceptives (e.g., hormone deficiency or treat- fort, lack of requirement for attention, and ment of acne or hirsutism). It is reasonable safety for use in women for whom estrogen for women who have coitus twice weekly or is contraindicated. Its major disadvantages more frequently to use oral contraceptives, are its expense, invasive insertion and re- unless there is some contraindication to moval, and frequency of associated irregular their use (see Tables 9-5 and 9-6). Oral con- bleeding. Although no changes in carbohy- traceptives have not been shown to alter drate metabolism, blood coagulation, or athletic performance. liver function have been reported, it is un- known whether Norplant contraception af- Failure rates for various contraceptive fects exercise performanceor endurance. methods are listed in Table 13-1.16 Choosing a Contraceptive DYSMENORRHEA The choice of an optimal contraceptive Dysmenorrhea is caused by myometrial agent for any athlete rarely should be af- ischemia during myometrial contractions fected by exercise habits but should include induced by prostaglandin F2a, which is pro- consideration of medical history and life- duced by the endometrium. Synthesis of this chemical can be prevented by any of several Table 13-1. FIRST-YEARFAILURE RATES prostaglandin synthetase inhibitors (Table OF BIRTH CONTROL METHODS 13-2). Lowest Typicalt Although many women have noticed less Reported* dysmenorrhea during exercise or training or both, most of these observations remain Female sterilization 0.0 0.4 anecdotal and unsupported by well-con- Male sterilization 0.0 0.15 trolled scientific studies. The nature of stud- Implant (Norplant) 0.0 0.04 ies involving exercise as the independent Injectable progestogen 0.0 0.3 0.0-1.1 3 Table 13-2. PROSTAGLANDIN INHIBITORS (Depo-Provera) 0.5-1.9 3 Birth control pill 4.2 12 Generic Name Brand Name Recommended IUD 2.1 18 Dose Condom 14-28 18-28 Diaphragm 18 Aspirin Naprosyn 650 mg every 4 Sponge 8 18 Naproxen h Cap 6.7 20 Anaprox, Withdrawal 2-14 21 Naproxen Anaprox-DS 500 mg, then 250 Periodic abstinence 0.0 85 sodium mg every 6-8 Spermicides 43 Motrin, Advil, h Chance Ibuprofen Nuprin Mefenamic acid 550 mg, then 275 *In the literature on contraceptive failure, the lowest re- Ketaprofen Ponstel mg every 6-8 ported percentage who experienced an accidental Orudis h or 550 mg pregnancy during the first year following initiationof every 12 h use (not necessarily for the first time) if they did not stop use for any other reason. 400 mg every 4-6 h tAmong typical couples who initiated use of a method (not necessarily for the first time), the percentage 500 mg, then 250 who experienced an accidental pregnancy during the mg every 6 h first year if they do not stop use for any other reason. 25-50 mg every Source: Modified from Hatcher et al,16 with permission. 6-8 h
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