Restoring the Severely Atrophic Maxilla

Miles 1a 1b 1c 1d Figure 1: 1a. Axial slice of 346 slices at the level of the condylar head. 1b. Axial slice of the same patient slightly higher up in the scan at the level of the sphenoid sinus. 1c. and 1d. Sagittal and coronal slices through the sphenoid region. CAT scans, PET scans, magnetic resonance To confound your decision-making, many imaging (MRI), ultrasonography, and nuclear “large volume” manufacturers claim that “you medicine scanning to assess their patient’s can do ALL of your imaging ONLY with a cone problems. Dentistry is gradually moving in a beam machine.” In my opinion, this is not true similar direction, especially with cone beam tech- and should never be considered because of two nology and cone beam “multifunctional” machines. factors I have previously discussed at length: The Journal of Implant & Advanced Clinical Dentistry 49

Miles 2a Figure 2: Images 2b acquired with SCARA 2c technology. All images taken on a panoramic machine (ProMax, Planmeca USA, Inc, Roselle, IL). 2a.“Panoramic bitewing” radiograph; 2b. Implant cross-sectionals; 2c. Tomographic images of the left TMJ condyle. 50 Vol. 1, No. 2 April 2009

Miles 3a 3b Figure 3: 3a. Axial slice of 500 slices at the level of the mid maxillary sinus showing 2 mucous retention cysts. 3b. Coronal slice near a posterior implant site showing the more medial mucosal lesion in the same patient possibly communicating with the inferior turbinate. namely, increased dose to children and reduced see these changes in the first case/example (Fig- productivity required for reconstructing an image ure 1) because of the increased area of coverage. like the panoramic.1-3 A perfect example of this Remember, you are not looking a single image, but is monitoring the status of deciduous and perma- rather 300-500+ slices in 3 planes. The examina- nent successor teeth in young children. When tion of these volumes, large or small, takes time. performing routine exams such as these, you must carefully weigh the risks of additional radia- With respect to the “large vs. small debate”, tion exposure in obtaining CBCT volume sets there seems to be a compromise on the horizon. when a simple panoramic image would suffice. Large volume manufacturers are moving towards a selectable FOV so that the operator can select Figure 3 shows some “small” FOV images a smaller region to fit the diagnostic task. Small and images from multi-functional machines. volume manufacturers, on the other hand, appear to be getting ready to offer machines with large In these examples, the dentist, in most cases, FOVs to attract customers like orthodontists who would be skilled enough to interpret the antral find- require larger areas for cephalometric analyses. ings. If nothing else, he or she would describe the lesions they found and refer the patient for an oto- The Types of Information in Each Scan laryngologic evaluation. A simple description of So what exactly is found in these scans? Back the changes seen would suffice as long as it was in late 2006, I published an article describing accompanied by informing the patient and referring the findings of the first 381 cone beam volumet- that patient to a specialist or back to their primary ric cases I examined for various radiology labora- care physician for further evaluation. It is harder to The Journal of Implant & Advanced Clinical Dentistry 51

Miles Table 1: Common Reportable Findings on CBCT Scans 1. Paranasal sinus disease such as mucous retention cysts, chronic sinusitis and blocked ostia 2. Enlarged adenoid and tonsillar tissues 3. Tonsilloliths 4. Deviated nasal septae and concha bullosa* (Figure 4) 5. Calci ed, elongated stylohyoid ligaments 6. Osteoarthritic changes on TMJ condyles 7. Osteoarthritic changes on cervical vertebrae 8. Missed dental conditions such as palatal root lesions, bone loss and implant perforations (usually because 3D imaging was not used) 9. Inferior alveolar nerve proximity to and contact of impacted third molars Table 2: Signi cant Findings tory services.4 Even now, after interpreting almost (number of cases in parentheses) 4,000 cases to date, I am impressed with the 1. Throat masses (4) amount of “reportable pathology” in these data 2. Vertebral tumors (2) volumes. Table 1 lists the most common findings 3. Fungus balls I have seen on the majority of scans I review while (aspergillosis), sphenoid sinus (2) Table 2 lists some of the more significant findings 4. Odontogenic cysts and tumors (6-10) that I have reported over the course of my career. 5. Calci ed plaques and medial It is important to evaluate the entire data volume. arterial calcinosis (approximately 30) The number of significant and reportable findings 6. Oro-antral stulae (more than 5) I have seen over the years support this concept. 7. Implant perforations (more than 20) 8. Cranial tumors (2) Potential Liability One of the biggest misconceptions in the den- tal profession is who “owns” the liability if a sig- nificant finding is missed during interpretation of a CBCT scan. Some of this confusion can be attributed to a so-called “mock trial” held at the 108th annual session of the American Asso- 52 Vol. 1, No. 2 April 2009

Miles 4a 4b Figure 4: An example of the anomaly “concha bullosa” in the middle turbinates. *Concha bullosa: Aeration of the middle turbinate, termed “concha bullosa,” is a common anatomical variant of intranasal anatomy. Of 320 patients evaluated for sinus disease with coronal CT, 34% had concha bullosa on at least one side. The overall incidence of inflammatory disease in the ostiomeatal complex in these symptomatic patients was not different between those with and without concha bullosa. However, there were many cases in which an abnormally large middle turbinate appeared to obstruct the ostiomeatal complex causing secondary infection of the ethmoid, frontal, and maxillary sinuses. Obstruction of drainage of the concha bullosa itself can lead to mucocele formation. Furthermore, the presence of a concha bullosa has important implications for the technique of endoscopic surgery used in the management of the sinus disease. ciation of Orthodontists in 2008. Following the To protect from this exposure, the scans session of the “Doctor’s Risk Management Pro- should be read by a trained practitioner.” 6 gram”, Ms. Elizabeth Franklin, a claims manager for the AAOIC (American Association of Ortho- This is prudent advice. In a recent article by dontists Insurance Company) wrote the following: trial lawyer Mr. Kevin Henry,7 at the 1st International Congress on 3-D Dental Imaging, California litiga- “Cone-beam scans are a relatively new form tion attorney Arthur Curly, who specializes in medi- of imaging available to the orthodontists to cal and dental malpractice, informed dentists that: enhance patient treatment. Many orthodon- tists, however, are not trained to read three “Dentists and team members are not dimensional scans. If the scans are not read licensed to treat medical problems or accurately and thoroughly, and incidental any other issues outside of the oral cav- findings are missed, the orthodontist can ity, so they are also not licensed to diag- assume a greater liability for failure to refer. nose conditions outside the oral cavity The Journal of Implant & Advanced Clinical Dentistry 53

Miles that are outside the scope of their dental region of interest (orthodontic planning for practice. Therefore, dentists can recom- example), and that patient release/consent mend 3-D imaging as an option without forms will absolve you from all responsibility fears that they could be liable for diag- from any outside specific narrowly tailored nosing everything seen on the image. usage. This, of course, is a legal rather than They are only responsible for those areas a medical question and the Board urges that are within the scope of their prac- you to consult your legal counsel for advice tice, dentistry: jaws and oral cavity.” before risking exposure to potential liabil- ity. However, you should always remem- Unfortunately, some dentists have taken this to ber that the Board views the use of CBCT mean that they don’t have to look at the data vol- under the rules applicable to radiographs. ume except as it pertains to their region of inter- Therefore, if you acquire a volume of data, est or the specific task for which they acquired you should be able to interpret the data the volume. If you read the assertion by Mr. Curly, for a complete and accurate diagnosis.” someone has to look at all of the data. The prev- alence of “occult pathology” is just too great. This, to me as a dentist and a radiolo- gist, seems like a prudent approach. Just For comparison, let’s consider that you have because the technique is new and novel, at had a preliminary chest x-ray taken to examine your least for dentistry, why would we NOT be heart for enlargement or hypertrophy of the mus- responsible for interpretation of the data? cle. Do you really think your physician or the radi- ologist would fail to look at the lung field as well in The first is that they are not comfortable with that chest film? By the same analogy, you would all the anatomy and potential pathology which may never consider examining only half of a panoramic reside in the volume data. This is a legitimate con- radiograph because only one lower third molar was cern and many colleagues have sought out special- thought to be present. Accordingly, why would ists in oral and maxillofacial radiology to help them. you think that no one has to look at the entire The second is that they do not want to “pay” the cone beam data volume when only an implant site added cost, or have the patient pay an “extra fee” is being assessed? If the patient was harmed to have a specialist look at the volume, because because you didn’t look at the full data volume or it might make the case “too costly” for the patient have someone look at the data for you, it is my firm and the dentist might lose the anticipated proce- opinion that you may be facing a future lawsuit. dure fee. This is self-serving and again, in my opin- ion, irresponsible behavior on the part of a dentist. In the Spring issue of the North Carolina State Board of Dental Examiners Newslet- I even know of a colleague who has a patient ter,8 Dr. Clifford Feingold, the editor, stated: sign a “refusal” document to have the cone beam volume read by a specialist. Regarding “informed “It is the Board’s understanding that some consent” and “informed refusal” of care or treat- CBCT manufacturers emphasize that the ment, a succinct explanation is presented in the machine may be used to evaluate a single May-June 2007 issue of The Reporter, a publication 54 Vol. 1, No. 2 April 2009

Miles of the Texas Medical Liability Trust (TMLT). In this the dentist say that he/she has fully informed the issue, Ms. Jane Holeman, vice-president of Risk patient? The very thought that they’ve received Management for the TMLT states the following:9 informed consent from the patient, a dental and medical necessity, before all the information is eval- “Implicit in and intrinsic to the concept uated and known is absurd. How can the patient of consent for treatment is the option of give or sign their “informed refusal” without having refusal. In Cruzan v Director, Missouri knowledge of all of the information in the x-ray? Department of Health, the U.S. Supreme Court ruled that all U.S. citizens have a con- CONCLUSIONS stitutional right to refuse unwanted therapy, a right residing in the due process clause Despite my rather sobering comments about the of the 14th amendment. Authorized surro- “Agony” of cone beam imaging, the interest, use, gates can exercise this right of refusal on and adoption of this modality is welcomed by the behalf of the incapacitated patients they dental profession. We benefit by better decision- represent. This right of refusal pertains making information, our patients benefit by more to all therapies, including life-sustaining precise surgical placement of implants and better therapies and artificial hydration and nutri- assessment of orthodontic, TMJ, and sinus prob- tion, without which patients will die.” All lems in addition to suspected and unsuspected patients have the right, after full disclo- pathology. We can expect improvement in hard- sure, to refuse medical treatment. This ware, software, detectors and knowledge as they can include patients who decline medi- relate to this impressive and much needed tech- cation, routinely miss office visits, defer nology. In the end, we can continue to bask in diagnostic testing, or refuse hospitaliza- the “Ecstasy” of Cone Beam Imaging, because tion. Physicians are then prohibited from it truly helps us all: both patient and clinician. proceeding with the intervention. “Prob- lems arise, however, when the patient or Disclosure the patient’s family later argues that they The author reports no conflicts of interest with anything mentioned within this were not given enough information to make article. an informed decision, or that the patient References lacked the capacity to make the decision…” 1. Miles D, Danforth R. A Clinician’s Guide to Understanding Cone Beam The final part of this statement holds the key to Volumetric Imaging. Academy of Dental Therapeutics and Stomatology Special this dilemma. How can a patient be expected to Issue 2007; 1-13. make an informed decision before they have all the 2. Miles D. The Future of Dental and Maxillofacial Imaging. Dent Clin N Am information? If the scan volume is not interpreted 2008; 52(4): 917–928. and the dentist lacks ANY information about poten- 3. Miles D. Color Atlas of Cone Beam Volumetric Imaging for Dental tial diagnoses and problems which might be in the Applications. Quintessence, Ch. 4-14 (pp 47-303), 2008. x-ray data, that is the “occult pathology”, how can 4. Miles D. Clinical Experience with Cone-Beam Volumetric Imaging: Report of Findings in 381 cases. US Dentistry 2006; 1(1): 39-42. 5. Zinreich S, Mattox D, Kennedy D, Chisholm H, Diffley D, Rosenbaum A. Concha bullosa: CT evaluation. J Comput Assist Tomogr 1998; 12(5): 778- 84. 6. Franklin E. “Doctor’s Risk Management Program.” 108th annual session of the American Association of Orthodontists. Denver, Colorado: May 2008. 7. Henry K. 10 tips from a trial lawyer. Dent Economics 2008; 98 (6). 8. Feingold C. Cone Beam Imaging. The Dental Forum, NC State Board of Dental Examiners Spring 2007. 9. Brockway L. When Patients Decline Treatment: Informed Refusal. The Reporter, Texas Medical Liability Trust; May-June 2007. The Journal of Implant & Advanced Clinical Dentistry 55

Byarlay

4% Articaine Use Byarlay in United States and Canadian Dental Schools Matthew R. Byarlay DDS, MS1 Abstract Background: Since the introduction and rise in dibular blocks, 68% reported only with faculty popularity of 4% articaine have come reports of approval and 11% restricted it for graduate stu- nerve injuries and paresthesias following mandibu- dents only. Other responses included restrictions lar blocks. This study examined how articaine is to surgery department and for supplemental use being used in educational institutions and if they only. Only 6% (2) of the respondents believed have had an increase in IAN and LN injury due to their institution has had a nerve injury during man- this product. dibular block anesthesia related to articaine, while 94% (31) had no such injury to report, and only Methods: An e-mailed survey questionnaire was one respondent reported inferior alveolar nerve sent to all U.S. and Canadian dental schools con- injury in 3 cases which could possibly be related cerning the availability of 4% articaine in their clin- to articaine use ics, restrictions of its use, and whether or not they had sustained any possible nerve injuries related Conclusion: Nerve injury due to articaine use was to its use. extremely low. Even with the lack of conclusive evidence that 4% articaine should not be used for Results: A total of 36 of the total 66 schools mandibular block analgesia, most of the reporting responded to the survey. 83% of the schools institutions have some form of restrictive protocol have articaine available but 79% have restrictions for its use in their clinics. placed on its use. 57% do not allow it for man- KEY WORDS: Articaine, local anesthesia, paresthesia, nerve injury, cytotoxicity 1. Assistant Professor, Department of Surgical Specialties, University of Nebraska Medical Center College of Dentistry, Lincoln, Nebraska The Journal of Implant & Advanced Clinical Dentistry 57

Byarlay BACKGROUND the fact that it was introduced only in the middle of the 8-year data collection period.2 Their con- Since its introduction into the United States in cluding statement read “there is a need for further 2000, articaine hydrochloride has gained wide- studies focused on the problem of neurotoxicity of spread popularity. This is likely due to its reported local analgesics with specific focus on articaine more profound anesthesia, faster onset, and suc- 4%. Until factual information is available, a pref- cess in patients who are difficult to anesthetize. It erence of other formulations to articaine 4% may has been available in Europe since 1976 and in be justified, especially for mandibular block anes- Canada since 1984. The approved formulation thesia.” In response to this study was a Letter to for the United States is a 4% solution with an epi- the Editor by Dr. Malamed which stated, “At this nephrine concentration of 1:100,000. With this time there exists absolutely no scientific evidence rise in popularity have come reports of nerve injury to support the concluding comment regarding and paresthesias following mandibular blocks. the use of other local anesthetics for mandibu- lar block analgesia in place of articaine 4%.”7 The mandibular block is one of the most common injections given by dental practitioners. Due to this continued concern over this par- Although it is frequently administered, it is more ticular formulation, we conducted a survey study of technically difficult than infiltration injections due to all U.S. and Canadian dental schools concerning its depth of needle penetration, reliance on varied their usage of this product in light of the apparent anatomical landmarks and placement of the anes- conflicting information. The purpose of this study thetic near the neurovascular bundle.3 Injury to the was to examine how 4% articaine is being used inferior alveolar nerve (IAN) or lingual nerve (LN) dur- in educational institutions and if they have had an ing this injection is reported to be low. Estimates of increase in IAN and LN injury due to this product. the prevalence of temporarily impaired IAN and LN function range between 0.15 and 0.54%.3,5 Per- MATERIALS AND METHODS manent paresthesia, although rare, has been noted. A list of all Canadian and U.S. dental schools The mechanism by which this injury occurs has was generated and an e-mail survey question- been the subject of much speculation. Proposed naire was sent to every Dean of Clinics at these mechanisms for paresthesia following injections institutions in the 2006-2007 academic year. The can include direct trauma to the nerve by the needle questions included in the survey were as follows: itself, hemorrhage into or around the neural sheath increasing pressure on the nerve leading to par- 1. Do you currently have articaine available esthesia, and neurotoxicity of the local anesthetic.1,6 for use in your clinics? A 2006 publication by Hillerup and Jensen 2. Are there any restrictions to the use of has lent support for the argument that local nerve articaine in your clinics? injury during a mandibular block anesthesia may be due to the neurotoxicity of the 4% articaine solu- 3. If so, please specify tion. This was based on the results of their study in a. Not allowed for mandibular blocks which nerve injuries caused by Articaine 4% cov- b. Must have faculty approval ered more than half of their sample size in spite of c. Graduate students only d. Other_______________ 58 Vol. 1, No. 2 April 2009

Byarlay 4, Has your institution had any nerve injuries calculation by the survey program. The results possibly related to Articaine use? from this question show 57% (n = 16) do not allow articaine for mandibular blocks, 68% (n 5. If lingual nerve involvement, approximately = 19) must have faculty approval, 11% (n = 3) how many cases? restrict use to graduate students only, and 28% (n = 8) added additional comments to answer 6. If inferior alveolar nerve involvement, this question. These responses included that it approximately how many cases? is only available through the surgery clinics, is for supplemental use only or that it is not avail- The questionnaire was re-sent mul- able at all. Eight of the respondents did not tiple times over several months to try and answer the question. For question #4, only 6% generate as many responses as possible. (n = 2) of the respondents believed their insti- tution has had a nerve injury during mandibular RESULTS block anesthesia related to Articaine, while 94% (n = 31) had no such injury to report. A total of Responses to the survey were returned from 36 3 respondents did not answer the question. For of the 66 total U.S. and Canadian dental schools question #5, regarding involvement of the lingual (table 1). In response to question (1), 83% (n nerve, 33 of the respondents skipped the ques- = 30 schools) of the respondents answered tion, and the other 3 did not know of any cases at “yes” with the remaining 17% (n = 6) answer- that time. For question #6, only one respondent ing “no”. In response to question 2, 79% (n = reported inferior alveolar nerve injury in 3 cases 29) answered “yes” and 21% (n = 6) answered which could possibly be related to articaine use. “no.” There was no response by 6 of the schools. For question #3, regarding what types of restric- tions are in place, multiple answers could be selected thus interfering with the percentage Table 1: Questionnaire Summary Question 1: Articaine available in clinic? Yes No 83% 17% Question 2: Restrictions on use? 79% 21% 43% 57% Question 3 (a): Allowed for mand blocks? 68% 32% 11% 89% Question 3 (b): Must have faculty approval? 6% 94% N/A 92% Question 3 (c): Graduate students only? 3 total cases N/A reported Question 4: Nerve injuries related to use? Question 5: Lingual nerve involvement? Question 6: Inferior alveolar nerve involvement? The Journal of Implant & Advanced Clinical Dentistry 59

Byarlay DISCUSSION with the incidence of non-surgical paresthesia being 1:765,000.8 Their conclusion agreed with The use of local anesthesia in dentistry is a nec- Haas and Lennon as articaine and prilocaine were essary procedure in the profession. According associated with the nerve injury more frequently to Malamed, it is estimated that dentists in the than any other local anesthetic. In 2005, Legarth United States administer more than 300 million conducted a retrospective review of reports of local anesthetic cartridges annually.1 These drugs paresthesia from 2002-2004 in Denmark. In that are considered very safe and nerve injury caused time span, 32 lingual nerve injuries were reported by injection of local anesthetics are considered with articaine being the anesthetic administered in very rare. With this being said, there can still be 88% of those cases.9 Most recently, Hillerup and nerve injury following a mandibular block, whether Jensen in 2006 looked at 54 injection injuries in by direct penetration from the needle, hemorrhage 52 patients caused by mandibular block analgesia. into the neural sheath or neurotoxicity of the local The lingual nerve was found to be injured more anesthetic itself. Our survey wanted to specifi- often (n = 42) than the inferior alveolar nerve (n cally examine if the use of 4% articaine was the = 12). Again, as in prior studies, was the obser- possible culprit in injury to the IAN or LN during a vation that 54% of the sensory impairment cases mandibular block. The results suggest that nerve were associated with the use of 4% articaine.2 injury due to articaine use was extremely low with only 1 respondent reporting possible nerve injury In vitro studies also seem to support the to this particular anesthetic in 3 cases. What is view that local anesthetics can be neurotoxic also particularly interesting is that even with the in a dose dependant manner. In 1976, a rat lack of conclusive evidence that 4% articaine study by Fink and Kish concluded that inhibi- should not be used for mandibular block analgesia, tion of rapid axonal transport is probably a usual most reporting institutions do report some form byproduct of nerve block with local anesthetics of restrictive protocol for its use in their clinics. such as lidocaine and that the effect was dose dependent.10 A review by Steen and Michen- Studies lending support to the view that 4% felder in 1979 of the neurotoxicity of anesthet- articaine causes a higher incidence of nerve injury ics also sites support for irreversible blocks of are numerous. A retrospective study by Haas and nerve trunks being a function of anesthetic con- Lennon found the overall incidence of paresthe- centration, exposure duration and pH.12 Lam- sia following local anesthetic administration to be bert in 1994 concluded that high concentrations very low, with only 14 cases being reported out of local anesthetics like 5% lidocaine have been of approximately 11,000,000 injections in 1993.4 shown to result in irreversible nerve conduction They concluded that this can be projected to block which was not found with 1.5% lidocaine.11 an incidence of 1:785,000 injections. Of par- ticular importance, however, was the fact that Contrary to the above studies is evidence from compared with other local anesthetics, a higher Malamed published at the time of articaine intro- incidence of parasthesia was found when artic- duction into the U.S. market. The studies pub- aine or prilocaine were used. A follow-up study lished in 2000 and 2001 examined the efficacy by Miller and Haas in 2000 found similar results and safety of 4% Articaine.13, 14 These were both 60 Vol. 1, No. 2 April 2009

Byarlay based on randomized, double-blind, multicenter that the reported incidence of nerve injury from trials where 1,325 patients received either 4% mandibular block anesthesia with 4% articaine is articaine with 1:100,000 epinephrine or 2% lido- extremely low with only 1 respondent reporting caine with 1:100,000 epinephrine for simple and possible nerve injury to this particular anesthetic complex dental procedures. The results of the in 3 cases. But due to the well publicized informa- efficacy study found no significant differences tion from retrospective reviews and associations between the two treatment groups. The results drawn between nerve injuries and 4% articaine, of the safety study found the overall incidence of it seems that most of the responding institutions adverse events was 22% for the articaine group keep this anesthetic under tight control. Its use and 20% for the lidocaine group. Paresthesia seems to be highly restricted, especially for man- was reported by 8 of the patients in the artic- dibular blocks, and in some cases, may not be aine group (0.9%) versus 2 of the patients in available at all. The lack of conclusive evidence on the lidocaine group (0.45%). The conclusion this subject will continue to have an impact on the from this study was that the adverse event pro- use of 4% articaine and will no doubt continue to file was similar between the groups. Addition- make its use in dental education controversial. ally, Malamed questions the strong conclusion from the Hillerup and Jensen paper in his letter Correspondence: to the editor in 2006 and continues to maintain Matthew Byarlay, DDS, MS that based on the available evidence, a state- University of Nebraska Medical Center ment such as “a preference of other formula- College of Dentistry, tions to articaine 4% may be justified, especially 40th and Holdrege for mandibular block analgesia” is not merited.7 Lincoln, NE 68583-0740 402-472-5289 fax There seems to be strong opinion on both Email: [email protected] sides of this discussion which adds to the inter- esting results from this survey. Our study shows Disclosure 5. Krafft TC, Hickel R. Clinical investigation into the 10.Fink BR, Kish SJ. Reversible inhibition of The author reports no conflicts of interest with incidence of direct damage to the lingual nerve rapid axonal transport in vivo by lidocaine anything mentioned in this article. caused by local anaesthesia. J Craniomaxillofac hydrochloride. Anesthesiology 1976;44(2):139- References Surg 1994;22(5):294-96. 45. 1. Malamed SF. Handbook of Local Anesthesia. 5th 6. Haas DA. Articaine and parestheia: 11. Lambert LA, Lambert DH, Strichartz GR. ed. St. Louis: Mosby, 2004. epidemiological studies. J Am Coll Dent 2006 Irreversible conduction block is isolated nerve 2. Hillerup S, Jensen R. Nerve injury caused by Fall;73(3):5-10. by high concentrations of local anesthetics. Anesthesiology 1994;80(5):1082-93. mandibular block analgesia. Int J Oral Maxillofac 7. Malamed SF. Nerve injury caused by mandibular Surg 2006;35(5):437-43. block analgesia. Int J Oral Maxillofac Surg 12. Steen PA, Michenfelder JD. Neurotoxicity 3. Harn SD, Durham TM. Incidence of lingual 2006;35(9):876-77. of anesthetics. Anesthesiology 1979 nerve trauma and postinjection complications in May;50(5):437-53. conventional mandibular block anesthesia. J Am 8. Miller PA, Haas DA. Incidence of local Dent Assoc 1990;121(4):519-23. anesthetic-induced neuropathies in Ontario 13. Malamed SF, Gagnon S, LeBlanc D. Efficacy of 4. Haas DA, Lennon D. A 21 year retrospective from 1994-1998. J Dent Res 2000;79(Special articaine: a new amide local anesthetic. J Am study of reports of paresthesia following local Issue):627. Dent Assoc 2000 May;131(5):635-42. anesthetic administration. J Can Dent Assoc 1995 Apr;61(4):319-20, 323-6, 329-30. 9. Legarth J. Lesions to the lingual nerve 14. Malamed S, Gagnon S, LeBlanc D. Articaine in connection with mandibular analgesia. hydrochloride: a study of the safety of a new Tandlaegebladet 2005;109:10. amide local anesthetic. J Am Dent Assoc 2001; 132(2):177-84. The Journal of Implant & Advanced Clinical Dentistry 61

Shumaker et al

The E ects of Periodontal Therapy on HelicobacShteumr aker et al pylori Clearance in Gastritis Patients: A Pilot Study N. Shumaker, DDS, MS1 1 2 3 3 Abstract Background: Prior studies suggest that dental Results: Experimental patients achieved a sta- plaque in periodontitis patients may be a res- tistically significant reduction in the mean plaque ervoir for Helicobacter pylori bacteria, nega- index from 1.25 pre-treatment to 0.63 post-treat- tively impacting gastritis treatment. This pilot ment (p = 0.004; <0.05). The control patient’s study evaluated whether scaling and root plan- plaque index remained relatively unchanged, with ing treatment could improve the clearance of 1.42 at baseline and 1.39 at the post-treatment H. pylori bacteria in patients with both H. pylori exam. The mean experimental group gastric H. gastritis and periodontitis. pylori levels were reduced from 266,306.43 cop- ies of H. pylori RNA/100 ng sample pre-treat- Methods: Four patients with H. pylori gastritis ment to 119.04 copies post-treatment. In the and chronic periodontitis were evaluated by both control patient, a pre-treatment H. pylori level of upper GI endoscopy and periodontal clinical and 188,474.37 copies was found, however the post- radiographic examination before and 8-12 weeks treatment level remained high at 8,643.93 copies. after gastritis treatment. Gastric biopsies were The control patient demonstrated a 72-fold higher harvested during both endoscopic examinations. residual H. pylori level after treatment compared Gastritis treatment consisted of the “triple-ther- to the experimental group. apy” H. pylori eradication regimen (two antibiotics and a proton pump inhibitor). Three experimental Conclusion: The findings of this pilot study sug- patients received scaling and root planing treat- gest that periodontal treatment, targeted at reduc- ment along with triple-therapy, while one control ing oral H. pylori levels, may result in improved patient received only oral hygiene instruction. Dur- clearance from the stomach during gastritis ing the periodontal evaluations the Silness plaque treatment. Further study with a larger number of index was assessed. Gastric tissue samples were patients is warranted. tested for H. pylori RNA levels using quantitative RT-PCR. Data trends were evaluated. KEY WORDS: Helicobacter pylori, periodontal disease, gastritis, peptic ulcer disease, dyspepsia, scaling and root planing 1. Department of Periodontics, Naval Postgraduate Dental School, National Naval Medical Center; Bethesda, MD 2. Department of Gastroenterology, National Naval Medical Center; Bethesda, MD 3. Department Medicine, Uniformed Services University School of Health Sciences; Bethesda, MD The Journal of Implant & Advanced Clinical Dentistry 63

Shumaker et al BACKGROUND sies for H. pylori. Patients with positive evalu- ation results are commonly treated with an oral Helicobacter pylori is a gram-negative, microaero- medication regimen known as “triple-therapy” philic, acidophilic organism, first described in that includes two antibiotics combined with a 1983 by Marshall and Warren.1 H. pylori infects proton pump inhibitor or bismuth for 14 days.2 human gastric tissues causing inflammation known After treatment, a second follow-up EGD proce- as H. pylori-induced gastritis.2 Gastritis symp- dure is recommended to verify clearance of H. toms include abdominal pain (dyspepsia), gastric pylori, since its persistence is associated with hemorrhage (which includes peptic ulcer disease), both further gastritis symptoms and the develop- nausea, reflux and loss of appetite. Infection rates ment of gastric carcinoma and lymphoma, which are reported at 20% for adults in the developed has a 5-year mortality rate of 50-75%.14 Triple world, and 90% in the developing world.2,3 H. therapy has been shown to achieve an 85-90% pylori is the reported cause of 70-90% of chronic clearance rate, however recurrence of infec- active gastritis cases and is responsible for 5% tion occurs in up to 25% of treated patients.15,16 of primary care physician visits annually in the United States.2,4 Treatment of H. pylori related Treatment for chronic periodontitis may gastrointestinal problems accounts for $3 bil- involve both non-surgical and surgical modali- lion dollars per year of US healthcare spending.5 ties. Non-surgical treatment involves a proce- dure known as scaling and root planing (SRP). Chronic periodontitis is an inflammatory dis- SRP is targeted at removal of bacterial plaque ease of the supporting structures of the teeth, and calculus from involved tooth crown and which affects 30% - 50% of the US population.6 root surfaces with the use specialized curettes It is caused by a convergence of dental plaque to create a root surface which promotes healing (a complex biofilm of over 500 types of bacteria) and control of disease.17 If SRP therapy is not with an aggressive host immune response that successful various surgical techniques may later leads to periodontal bone resorption, soft tis- be necessary to restore periodontal health.17 sue attachment loss, tooth mobility and eventual loss.7,8 As periodontitis initiates and progresses, Prior studies have suggested that dental deep periodontal pocketing with anatomic bony plaque in chronic periodontitis patients may and soft tissue defects result, providing an eco- be a reservoir for H. pylori bacteria, which logical niche where plaque can further accumu- may reduce the success of gastritis treatment. late undisturbed, inaccessible by oral hygiene Chronic periodontitis patients have been found practices.9,10 In recent studies, a positive asso- to harbor high levels of H. pylori in their den- ciation has been found for chronic periodontitis tal plaque in as many as 87%-97% of sample as a risk factor for several systemic diseases sites.18,19 These patients also demonstrate com- including cardiovascular disease, diabetic gly- paratively higher levels of H. pylori in their den- cemic control, and obstetric complications.11-13 tal plaque compared to periodontally healthy patients.20,21 Importantly, the treatment of gastric Treatment for H. pylori-induced gastritis H. pylori with triple-therapy antibiotics has been involves evaluation by an upper GI endoscopy found to have very little effect on oral H. pylori (EGD) procedure and testing of gastric biop- 64 Vol. 1, No. 2 April 2009

Shumaker et al levels found in dental plaque.22,23 Furthermore Figure 1: Histologic view of H. pylori bacteria in gastric the presence and persistence of H. pylori in the mucosa. oral cavity has been associated with reduced clearance of gastric H. pylori during gastritis Camplobacter-like organism test (CLO), four treatment.24 Despite these findings, no currently were submitted for histological examination published study has investigated whether an using special Steiner stains for H. pylori, and intervention of periodontal therapy, targeted at the remaining two were placed in RNA Later® reducing oral H. pylori levels, in conjunction with (Applied Biosystems; Foster City, CA), RNA sta- gastritis treatment might help to increase the bilizing agent and stored at -20 degrees Celsius success of H. pylori clearance from the GI tract. for later experimental testing using PCR tech- niques. Of these 50 patients, eight patients were Therefore, a prospective randomized con- found to be positive for gastric H. pylori from the trolled pilot study was completed at the National biopsies collected during the EGD procedure. Naval Medical Center; Bethesda, MD, to evalu- ate the effects of non–surgical periodontal The eight H. pylori positive patients were treatment (scaling and root planing) on the referred within one week to the Periodontics clearance of H. pylori bacteria from the stom- Department at the Naval Postgraduate Dental ach mucosa in patients diagnosed with both H. School, Bethesda, MD (NPDS) for a periodon- pylori-related gastritis and chronic periodontitis. tal evaluation. During the periodontal examina- tion, pocket depths (PD) and clinical attachment MATERIALS AND METHODS levels were recorded (using the cemento-enamel junction as a fixed reference) and vertical bitew- The study protocol was reviewed and approved ing radiographs were examined. Dental plaque by the Responsible Conduct of Research levels were assessed in each patient using the Department at the National Naval Medical Cen- Plaque Index system described by Silness and ter (NNMC). This approval was granted after Loe25,26 on 4 surfaces per tooth. The plaque being reviewed by the Scientific Review Panel index uses a scale of 0-3 with 0 representing no and the Institutional Review Board. All patients identified as candidates for the study were pro- vided thorough informed consent both verbally and in writing regarding the risks and benefits of participation. 50 patients with gastroentero- logical symptoms suggestive of dyspepsia or peptic ulcer disease (PUD) were consented for the study in the Gastroenterology department of the NNMC and underwent upper GI endoscopy (EGD) procedures under conscious sedation to test for H. pylori bacteria in the stomach. During the EGD, eight gastric biopsies were harvested for H. pylori testing. Two were tested using the The Journal of Implant & Advanced Clinical Dentistry 65

Shumaker et al dental plaque and 3 representing heavy plaque reassessment of the plaque index to reevalu- accumulation. The mean plaque index across all ate the condition of the periodontium post-triple tooth surfaces was calculated for each patient therapy. The control patient then received scal- and recorded. Of the eight H. pylori positive ing and root planing after the second periodontal patients, four were found to also have peri- examination, as this marked the end of the study. odontal disease (defined as >2 pocket depths >4mm with bleeding on probing and evidence of At the time of collection, gastric tissue sam- radiographic bone loss). These four patients, of ples were placed immediately in sterile Eppen- the original fifty enrollees, therefore comprised dorf tubes filled with an RNA stabilizing solution the study sample. Three of these four patients (RNA Later®, Ambion, Inc.). Specimens were received scaling and root planing (SRP) ther- stored at -20o C until processing. For pro- apy (single session), as well as oral hygiene cessing, specimens were transported to the instruction on tooth brushing and dental floss Digestive Diseases Research Division of the techniques at the initial periodontal exam (exper- Uniformed Services University of the Health imental group). One patient received only oral Sciences, Bethesda, MD, subjected to RNA hygiene instruction and did not undergo SRP extraction under sterile endoribonuclease-free therapy after the initial exam (control patient). conditions, and stored at -70o C until testing. When all samples were collected and extracted, Immediately after this visit all patients absolute quantitative real-time RT-PCR (QRT- received a prescription “triple-therapy” regimen PCR) was performed in a single-tube reaction aimed at eradication of H. pylori. This consisted with a TaqMan One-Step RT-PCR Master Mix of a 14 day oral regimen of two antibiotics, which Reagents kit (Applied Biosystems) designed for included Clarithromycin (500mg taken bid) with reverse transcription (RT) and polymerase chain either Amoxicillin (1 gram taken bid) or Metron- reaction (PCR) in a single buffer system and an idazole (500mg taken bid), and Omeprazole (20mg taken bid), a proton-pump inhibitor. Eight 1.42 1.39 to twelve weeks after completion of the “triple- therapy” regimen, all four patients returned to *Statistically significant reduction the Gastroenterology department of NNMC (P=0.004, Paired T-test) where a second EGD procedure was performed to verify clearance of H. pylori from the stomach. Eight gastric tissue samples were harvested and stored in the same manner as the first EGD, including two post-treatment samples in RNA Later for PCR testing for H. pylori. Within one week after the follow-up EGD procedure patients returned to the Periodontics Department at NPDS for a follow-up examination including reevaluation of periodontal pocket depths and 66 Vol. 1, No. 2 April 2009

Shumaker et al ABI PRISM 7500 Sequence Detection System H. pylori (Applied Biosystems, Foster City, CA). Bacterial load was reported as copies of H. pylori RNA estingly, this patient continued to have dyspeptic per 100 ng of total RNA sample. Data analy- symptoms despite treatment. In comparing the sis was completed with descriptive and inferen- residual post-treatment H. pylori levels between tial statistics using a student’s T-test to evaluate the two groups, the control group demon- the significance of periodontal therapy on H. strated a 72-fold higher residual H. pylori level pylori reductions achieved in this patient group. compared to the experimental group (Figure 2). RESULTS DISCUSSION A mean pre-treatment plaque index for the The results of this small pilot study suggest a experimental group patients (n=3) was found trend which may indicate that scaling and root to be 1.25 (± 0.10). The pre-treatment plaque planing treatment could increase the clearance index for the control patient (n=1) was 1.42. of H. pylori from the gastric mucosa during treat- The experimental patients all achieved a sta- ment of H. pylori-related gastritis. The control tistically significant reduction in their plaque patient had a high level of residual infection at the index after scaling and root planing (p = 0.004; post treatment EGD (8,643.93 copies H. pylori <0.05 Paired T-test), with a post-treatment RNA/100ng sample) in comparison to the exper- mean plaque index of 0.63 (±0.17). The con- imental patients (mean=119.04 copies H. pylori trol patient, who did not receive scaling and RNA/100ng sample) by a magnitude of 72 fold. root planing, showed a plaque index similar to This reduction appeared to correlate to a statis- baseline of 1.39 at the followup visit (Table 1). tically significant drop in the plaque index in the experimental patients which resulted from scal- Experimental group patients demon- ing and root planing therapy in conjunction with strated mean pre-treatment H. pylori levels of H. pylori eradication treatment. While the actual 266,306.43 copies of H. pylori RNA/100 ng of reduction in gastric H. pylori was not found to sample (±134,212.66), with a mean post-treat- ment level of 119.04 copies/100 ng of sample (±202.64). This appears to be a large reduc- tion, however, it was found only to approach statistical significance (p=0.07) due to the high variability in H. pylori levels between each patient and the small number of patients who met the study criteria. The control patient dem- onstrated a pre-treatment H. pylori level of 188,474.37 copies of H. pylori RNA/100ng of sample. At the post-treatment EGD this patient still harbored a high level of residual H. pylori with 8,643.93 copies persistent (Table 2). Inter- The Journal of Implant & Advanced Clinical Dentistry

Shumaker et al be statistically significant, the magnitude of the the emergence of putative pathogens implicated comparative reduction in the experimental group in the pathogenesis of periodontitis.27,28 These suggests a trend which supports our hypoth- include species such as Treponema denticola, esis. Statistical analysis in this pilot study was Porphorymonas gingivalis, Tanerella forsythia, challenged by the small sample size obtained Campylobacter rectus, and Fusobacterium after 13+ months of data collection. Addition- nucleatum.29 Several studies have suggested ally, the presence of only one control patient that there is an ecological niche for H. pylori in made statistical comparison between groups dental plaque. Okuda (2003) found that Por- difficult. Regardless, the trend suggested by the phorymonas gingivalis and Fusobacterium results of this pilot study is promising and high- nucleatum in dental plaque strongly coaggre- lights a need for further research on this subject. gate with H. pylori, and may actually entrap H. pylori cells in the dental biofilm.30,31 While saliva Development of dental plaque occurs within contains immuno-defensive mechanisms, such hours of mechanical removal by oral hygiene or as secretory IgA, the value of these defenses professional instrumentation, and proceeds to may be limited against H. pylori since many develop into an increasingly organized biofilm. authors have found H. pylori is present in saliva Sequential colonization of dental plaque leads to H. pylori Vol. 1, No. 2 April 2009

Shumaker et al samples.22,23,31 Additionally saliva does not mission also have been shown.36 In gastri- penetrate into subgingival areas including peri- tis patients, vomiting or reflux may facilitate odontal pockets of periodontitis patients, due infection of the dental plaque from the stom- to the constant outward flow of gingival crev- ach, however this does not account for how H. icular fluid which increases with inflammation.32 pylori entered the stomach in the first place. Regardless of how it arrives in the oral cavity, Our study did not include sampling and the presence of H. pylori may serve as an oral analysis of dental plaque samples for the pres- reservoir which resists clearance by antibiot- ence of H. pylori. Since prior studies by other ics during triple-therapy antibiotic treatment.22-24 researchers using PCR techniques have This persistent H. pylori in dental plaque may shown its presence with great frequency, we be constantly translocated to the gut during chose only to measure the quantitative dental eating and swallowing, facilitating reinfection. plaque reduction with SRP using the plaque index.19-23 Earlier studies using culture tech- The findings of this small pilot study suggest niques had mixed findings on the presence of that that reducing the level of dental plaque in H. pylori in dental plaque, and it is only with patients with periodontitis may increase the the advent of PCR detection techniques that it success of H. pylori eradication with the triple- has been reliably detected in plaque samples.33 therapy regimen in the treatment of H. pylori- induced gastritis. Conversely, the persistence Compliance with any oral medication regi- of dental plaque in untreated chronic periodon- men can confound study data. In this study, titis patients may serve as an H. pylori reservoir verification of compliance with triple-therapy which may reduce the success of such treatment. was not assessed. Studies on patient compli- ance with oral medications appears to decrease CONCLUSION with increasing complexity of the regimen (ie. a single antibiotic would have better compli- This pilot study suggests that there may be ance than three different medications in tri- enhanced H. pylori clearance in patients ple-therapy).34,35 However the medical and with both H. pylori gastritis and chronic dental literature support that patient compli- periodontitis when non-surgical periodon- ance is highest when patients perceive a dis- tal treatment is rendered as an adjunct to ease risk exists or have symptoms resulting the triple-therapy regimen. Further investiga- from a disease which the believe will improve if tion with a larger number of patients is neces- they follow treatment recommendations.35 All sary to better understand this relationship patients in this study had symptomatic dyspep- sia or peptic ulcer disease. Therefore, it may Correspondence: be expected that they had reasonable com- Nicholas D. Shumaker DDS, MS pliance with the recommended medications. c/o Research Department, Naval Postgraduate Dental School, Building 1, 8901 Wisconsin Ave Acquisition of H. pylori appears to occur Bethesda, MD 20889-5600 person to person via an oral-oral route, but drinking water, animal, and food borne trans- The Journal of Implant & Advanced Clinical Dentistry 69

Shumaker et al Acknowledgements 12. Lin D, Moss K, Beck JD, Hefti A, Offenbacher 25. Silness J, Loe H. Periodontal disease in The authors would like to extend a special thanks S. Persistently High Level Of Periodontal pregnancy; II. Correlation between oral hygiene to the following individuals who contributed to the Pathogens Associated With Preterm and periodontal condition. Acta Odontol development and completion of this pilot study: Pregnancy Outcome. J Periodontol Scand. 1964;22:112-135. John Mumford, DDS, MS; Dong Lee, MD; Rebecca 2007;78:833-841. Christensen, MD and Mary E. Neill, DDS, MS. 26. Loe H. The gingival index, the plaque index, 13. Rodrigues DC, Taba M, Novaes AB, Sousa and the retention index systems. J Periodontol. Disclosure SLS, et al. Effect of non-surgical periodontal 1967;36:610-616. The authors report no conflicts of interest with therapy on glycemic control in patients with anything mentioned in this article. type 2 diabetes mellitus. J Periodontol 2003 27. Offenbacher S, Costopoulos SV, Odle BM, 74(9): 1361-1367. Van Dyke TE. Microbial colonization patterns Disclaimer of loosely adherent subgingival plaque in “The views expressed in this abstract are those of 14. Hsu PI, Lai KH, Hsu PN, Lo GH, et al. adult periodontitis. J Clin Periodontol.1988 the author and do not necessarily reflect the official Helicobacter pylori infection and the risk of Jan;15(1):53-9. policy or position of the Department of the Navy, gastric malignancy. Am J Gastroenterol. 2007 Department of Defense, nor the U.S. Government” Apr;102(4):725-30. 28. Loe H. Experimental gingivitis in man. J Periodontol 1965; 36:177-187. References 15. Ong SP, Dugan A. Eradication of Helicobacter 1. Marshall BJ, Warren JR. Unidentified curved pylori in clinical situations. Clin Exp Med. 2004 29. Socransky SS, Haffajee AD, et al. Microbial Sep;4(1):30-8. complexes in subgingival plaque J Clin bacilli in the stomach of patients with gastritis Periodontol. 1998; 25:134-144. and peptic ulceration. The Lancet. 1984 Jun 16. Xia HX, Talley NJ, Keane CT, O’Morain CA. 16;1(8390):1311-1314. Recurrence of Helicobacter pylori infection 30. Andersen RN, Ganeshkumar N, Kolenbrander after successful eradication. Dig Dis Sci. PE. Helicobacter pylori adheres selectively to 2. Talley NJ, Vakil NB, Moayyedi P. American 1997;42(9):1821-1834. fusobacterium spp. Oral Microbiol Immunol. Gastroenterological Association technical review 1998;13:51-54. on the evaluation of dyspepsia. Gastroenterol. 17. American Academy of Periodontology 2005;129:1756-1780. Parameters of Care. Parameter on chronic 31. Okuda K, Kimizuka A, Nakagawa T, Ishihara periodontitis with advanced loss of periodontal K. Ecological and immunopathological 3. Taylor DN, Blaser MJ. The epidemiology of support. J Periodontol 2000;71:856-858. implications of oral bacteria in Helicobacter Helicobacter pylori. Epidemiol Rev. 1999;13:42- pylori-infected disease. J Periodontol. 59. 18. Dowsett SA, Eckert GJ, Kowolik MJ. 2003;74:123-128. Helicobacter pylori infection in indigenous 4. Feldman M, Scharschmidt M, Sleisenger families of Central America: Serostatus and 32. Hancock EB, Cray RJ, O’Leary TJ. The H, editors. Sleisenger and Fordtran’s oral and fingernail carriage. J Clin Microbiol. relationship between gingival crevicular fluid gastrointestinal and liver disease: 1999 Aug:2456-2460. and gingival inflammation: A clinical and Pathophysiology/diagnosis/management. 6th ed. histologic study. J Periodontol. 1979;50:13-19. Philadelphia: WB Saunders; 1998: p 604-619 19. Song Q, Lange T, Spahr A, Adler G, Bode G. Characteristic distribution pattern of 33. Dowsett SA, Kowolik MJ. Oral Helicobacter 5. Sonnenberg A, Everhart JE. Health impact Helicobacter pylori in dental plaque and saliva pylori: Can we stomach it?. Crit Rev Oral Biol of peptic ulcer in the United States. Am J detected with nested PCR. J Med Micro. Med. 2003;14(3):226-233. Gastroenterol 1997;92:614-620. 2000;49:349-353. 34. Greenberg RN. Overview of patient compliance 6. Albandar JM, Brunelle JA, Kingman A. 20. Umeda M, Kobayashi H, Takeuchi Y, Hayashi with medication dosing: A literature review. Clin Destructive periodontal disease in adults 30 J, et al. High prevalence of Helicobacter Ther. 1984;6(5):592-599. years of age and older in the United States, pylori detected by PCR in the oral cavities 1988-1994. J Periodontol. 1999 Jan;70(1):13- of periodontitis patients. J Periodontol. 35. Wilson TG. Compliance: A review of the 29. 2003;74:129-134. literature with possible applications to periodontics. J Periodontol. 1987;58:706-714. 7. Moore WE, Moore LV. The bacteria of periodontal 21. Souto R, Columbo AP. Detection of diseases. Periodontol 2000. 1994;5:66. Helicobacter pylori by polymerase chain 36. Nabwera HM, Logan RPH. Epidemiology of reaction in the subgingival biofilm and saliva Helicobacter pylori transmission, translocation, 8. Genco RJ. Host responses in periodontal of non-dyspeptic periodontal patients. J and extragastric reservoirs. J Physiol diseases: current concepts. J Periodontol. 1992 Periodontol. 2008 Jan;79(1):97-103. Pharmacol. 1999;50(5):711-722. Apr;63(4 Suppl):338-55. 22. Gebara EC, Faria CM, Pannuti C, Chehter L, et 9. Carranza FA, Newman MG, Takei, HH. al. Persistence of Helicobacter pylori in the oral Carranza’s Clinical Periodontology. 9th ed. cavity after systemic eradication therapy. J Clin Philadelphia: WB Saunders. 2002: p. 96-112. Periodontol. 2006 May;33(5):329-33. 10. Page RC, Offenbacher S, Schroeder 23. Czesnikiewicz-Guzik M, Loster B, Bielanski W, HE, Seymour GJ, et al. Advances in the Guzik TJ, et al. Implications of oral Helicobacter pathogenesis of periodontitis; summary of pylori for the outcome of its gastric eradication developments, clinical implications and future therapy. J Clin Gastroenterol. 2007 directions. Periodontol 2000. 1997;14:216- Feb;41(2):145-51. 248. 24. Miyabayashi H, Furihata K, Shimizu T, Ueno I, 11. Scannapieco FA. Systemic effects of et al. Influence of oral Helicobacter pylori on periodontal diseases. Dent Clin North Am. the success of eradication therapy against 2005 Jul;49(3):533-50 gastric helicobacter pylori. Helicobacter. 2000;5(1):30-36 Vol. 1, No. 2 April 2009

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