Volume 81 Number 5

Case Report
Management of a Perplexing Sinus Lift Complication
Gary Greenstein* and John Cavallaro Jr.*

Background: This case report describes a dilemma that occurred after a maxillary right lateral window sinus lift was performed. The patient developed a gnawing pain in the sinus region but manifested no signs of sinusitis, and the subjacent teeth were asymptomatic. Differentiating between a pain that could be originating in the maxillary sinus or adjacent premolars was problematic. Methods: After several weeks, a CT scan revealed no signs of sinusitis, despite the patients belief that her discomfort was caused by her sinus lift. By the process of elimination, the decision was made to extract subjacent, asymptomatic premolars that had 50% bone loss and were previously endodontically treated. Results: Extraction of asymptomatic premolars resulted in total elimination of her pain. Conclusions: A differential diagnosis with regard to the source of the patients pain had to be arrived at by the process of elimination rather than by validation. Conrmation that there was no sinus infection facilitated making the decision to remove asymptomatic premolars. J Periodontol 2010;81:776-782. KEY WORDS Bone regeneration; case report; complications; dental implants; maxillary sinus; sinusitis; wound healing.

lateral wall sinus lift is a method to augment the posterior ridge when the crestal alveolar bone subjacent to the maxillary sinus is decient and cannot support a dental implant.1 After ap elevation, a lateral window is created in the buccal plate of bone, the schneiderian membrane is elevated, and a bone graft is placed in the space created by membrane elevation. This is a routine procedure; however, complications can occur. The incidence of sinus infections is around 3%, despite administration of antibiotics.2 Recently, a sinus lift done by one of the authors (GG) resulted in a patient having discomfort for 3 months until several perplexing issues were resolved. This case report describes steps taken to diagnose and eliminate the patients pain. PATIENT MEDICAL AND DENTAL HISTORY The patient was a 57-year-old, medically healthy, white woman with a long history of being a periodontal patient. She was treated initially in 1987 for chronic severe generalized periodontitis (surgical and nonsurgical therapy). Subsequently, the patient remained in maintenance every 3 months, and other periodontal procedures were performed as needed. In June of 2009, she desired to prosthetically restore sections of her mouth. Because of lack of alveolar bone in the maxillary right region, a sinus lift was performed in preparation for placement of an implant at site #3. In the maxillary right quadrant, teeth #1 and #2 were missing and teeth #4 and #5 had 50% bone loss (Fig. 1). The maxillary premolars (#4 and #5) were previously endodontically treated (12 and 15 years ago, respectively), restored with crowns, and tooth #5 had an apicoectomy 10 years ago. The teeth were functional and asymptomatic. Both premolars had shallow probing depths (2 to 3 mm; there was 5 mm of recession) and class I mobility (1 mm hypermobility). Before the sinus lift, treatment options were discussed with the patient, which included removing teeth #4 and #5 and expanding the sinus lift to plan for a prosthesis that would include replacement of teeth #3 through #5. She desired to retain teeth #4

* Formerly, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, NY. Private Practice, Surgical Implantology and Periodontics, Freehold, NJ. Private Practice, Surgical Implantology and Prosthodontics, Brooklyn, NY.

doi: 10.1902/jop.2010.090639

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July 10, 2009 She indicated that the gnawing pain at night comes and goes. The antibiotic was continued for another week. July 13, 2009 She still had discomfort. There were no signs of sinusitis. Teeth #4 and #5 were asymptomatic to percussion and palpation, probing depths were shallow, and there was no increased hypermobility on teeth #4 and #5. The teeth Figure 1. were transilluminated to check CT (panoramic view) of the maxillary right quadrant depicting a clear maxillary right sinus before the sinus lift was for a vertical root fracture, performed. R = right; L = left. and the patient was asked to bite on a tongue blade in different positions to check for a fracture. The patient was referred for an endand #5. Previously, tooth #6 was replaced with a denodontic consultation. The endodontist indicated that tal implant. there was no pathosis on teeth #4 and #5 and no apparent endodontic reason for the patients pain. CHRONOLOGY OF TREATMENT June 3, 2009 A lateral window sinus lift was performed in the maxillary right posterior region. The procedure was uneventful and proceeded without difculty. The membrane was elevated without creating a perforation and the postoperative panoramic radiograph indicated that the sinus graft material was well contained (Fig. 2). The inserted graft material was demineralized bovine bone (hydrated with sterile saline) and a collagen barrieri was placed over the lateral window. The patient was prescribed amoxicillin, 2 g 1 hour before the procedure, and continued taking amoxicillin, 500 mg tid, for 7 days. June 10, 2009 The patient reported no problems at a routine postoperative appointment. June 17, 2009 She complained of hypermobility and sensitivity on tooth #4. The tooth was equilibrated, and her discomfort was eliminated. July 3, 2009 She had discomfort. Teeth #4 and #5 were equilibrated. July 5, 2009 She described gnawing pain in the sinus area during the evening. A panoramic radiograph was taken (Fig. 3). The sinus was clear. There were no clinical symptoms of sinusitis. Metronidazole, 500 mg tid for 7 days, was prescribed as a precautionary measure. July 19, 2009 Her discomfort persisted; it was relieved with analgesic at night. There were still no clinical signs of pathosis. She was referred for an oral surgery consult. It was suggested to remove the sinus graft because when the lateral wall of the graft was pressed, she felt minor soreness. The patient did not want to do that, and the authors believed that without clinical signs of sinusitis or an intraoral infection, there was no justication to remove the graft. Clindamycin was prescribed but the patient developed hives in 1 day, so the drug was discontinued. July 26, 2009 Her discomfort continued, and she manifested no clinical signs of pathosis. The patient was prescribed methylprednisolone# and amoxicillin to resolve all issues. In actuality, this was shotgun therapy because the etiology of the problem was undiagnosed. August 3, 2009 The patients pain subsided for 5 days and then resumed. She was referred for a CT scan, which she did not immediately obtain. Consideration was given to referring the patient to an otolaryngologist. However, the patient did not have a problem before the sinus lift, there were no symptoms of a sinus infection, the graft was well contained, and it was believed that the etiology of the patients problem was of dental origin.
i # Bio-Oss, Osteohealth, Shirley, NY. BioMend, Zimmer Dental, Carlsbad, CA. Tylenol 3, Ortho-McNeil-Janssen Pharmaceuticals, Inc., Titusville, NJ. Medrol dose pack, Pzer US Pharmaceuticals, New York, NY.

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gauze. Each time her pain was temporarily relieved for 1 or 2 days. September 2 and 7, 2009 The socket was retreated with irrigation and eugenol on gauze. September 12, 2009 The patient was comfortable. She had no more discomfort. DISCUSSION The patient was completely comfortable 3 months after the sinus lift. There were several aspects of this case that made it difcult to expeditiously eliminate the patients discomfort. Namely, it was not easy to identify the source Figure 2. of her pain; it was most likely Panoramic radiograph on the day that the sinus lift was placed. It demonstrates a well-contained sinus graft. either from an infected maxillary right sinus or her maxillary right premolars were August 9, 2009 referring pain to the sinus region. Removal of the sinus Her gnawing pain in the evening continued. graft or the teeth without validating the source of the August 15 and 16, 2009 discomfort was undesirable because both procedures On August 15, the patient went for a CT scan. She was had negative consequences and might not eliminate seen in the ofce the next day, August 16. The scan her pain. demonstrated that the sinus graft was contained, Initially, it was believed that her distress was caused and the sinus was clear (Fig. 4). At this juncture, by traumatic occlusion on the maxillary right bicusthe patient wanted the sinus graft removed because pids, which were slightly hypermobile after the sinus she wanted her pain-free life back again. It was suglift. She manifested no signs of distress after the pregested to retain the graft, because it looked ne and molars were occlusally equilibrated. Two weeks later, there were no signs of sinusitis. Furthermore, it was she related that the teeth felt high, and she had recommended that teeth #4 and #5 be removed, dea gnawing pain. Following her second occlusal adjustspite the fact that they were asymptomatic on clinical ment, the teeth were asymptomatic, but the gnawing and radiographic inspection. In consultation with the pain persisted. She described it as if someone was patient, it was decided to remove these teeth, one at putting a screw into her bone, which was interpreted a time. to suggest the possibility of a sinusitis. A panoramic lm was obtained, which demonstrated that the sinus August 21, 2009 graft was contained and the sinus was clear (Fig. 2). Tooth #5, the tooth that had the apicoectomy, was reTo rule out the possibility of a sinus infection, the moved rst. The next day she reported her discomfort patient was visually inspected and palpated intraorwas not eliminated. ally and extraorally at each appointment. When she August 23, 2009 bent over there was no pain, indicating an absence Tooth #4 was extracted. of excess uids in the sinus. Her continuing discomfort, despite no appearance of a sinus infection (swellAugust 25, 2009 ing, pain on palpation), was puzzling. There was no She was in extreme pain. She had a local osteitis at site purulent discharge from the nostrils. A differential di#4. The socket was irrigated with saline and treated agnosis was confounded by the fact that the two prewith eugenol and gauze. Her pain was eliminated. molars (teeth #4 and #5) manifested no signs or August 26 and 28, 2009 symptoms of pathosis clinically or radiographically On both days, she had pain from the alveolus. The (Figs. 5 and 6) after her occlusal equilibration. The socket was irrigated and retreated with eugenol on teeth were asymptomatic on percussion, luxation,
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and buccal plate palpation. The probing depths around these teeth were shallow and radiographically there was no appearance of radiolucency. Transillu-

mination3 and occlusal testing4 for a fracture were negative. There was no swelling or a stulous tract indicating apical pathosis. A condition referred to as maxillary sinusitis of dental origin was considered in the differential diagnosis,5 and occurs when a dental infection causes destruction of the cortical bone and extends into the sinus. However, besides intermittent discomfort, the patient did not manifest signs of a sinus infection, the teeth were asymptomatic, and the radiographs revealed intact cortical bone apical to the premolars on a periapical radiograph (Fig. 5) and on the CT scan (Fig. 6). The bicuspids were endodontically treated many years ago, and clinical and radiographic assessments provided no information to suggest that Figure 3. Panoramic radiograph taken 4 weeks after the sinus graft was placed, indicating that the sinus area was the teeth were inducing siclear and that the graft was well contained. nusitis. Another symptom

Figure 4.
CT scan conrms that the sinus was clear, and the graft was well contained. R = right. Horizontal Lines (Red and Blue) indicate cross sections available for viewing. Horizontal Lines (Blue) indicate height of anatomy available for viewing in cross-sections.Tick Dist = Distance in mm from the most coronal aspect of the scan, which is 0; 100.00 = 100mm from top of scan; 120 = 120mm from top of scan. 779

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considered was the patients statement that the pain was worse at night. It was recognized that posture can affect blood pressure; when a patient lies down, there is less gravitational pull and a reduced inuence of the baroreceptor system, which can result in increased perfusion pressure at an inamed site.6 Thus, the increased pain at night and a throbbing sensation had a physiologic basis, but did not help differentiate between sinus or tooth-derived pain. The patients discomfort was relieved at night with ibuprofen, 600 mg, or acetaminophen. The possibility that there were trigger points associated with a neuralgia that would induce her distress was assessed and resulted in no atypical ndings.7 The only sign of discomfort noted was when the lateral wall of the sinus graft was pushed, she stated it felt sore. The soreness was minor and could be attributed to dissolution of a resorbable barrier over a site where the lateral window osteotomy was performed. In the maxilla, pain is frequently referred from the maxillary sinus to teeth because of the close anatomic association between the oor of the sinus and roots of maxillary teeth.8,9 In particular, when a patient has al-

Figure 5.
Periapical lms of teeth #4 and #5 demonstrate that there was an intact cortical plate of bone around the apices of the premolars.

Figure 6.
CT scan of teeth #4 (sections 24 and 22) and #5 (sections 20 and 18) conrms that the apices of the premolars did not penetrate into the sinus and did not manifest any apparent radiolucencies. 780

lergies, the lining of their sinus tissues can become inamed, and the patient perceives the discomfort as dental in origin, but it may be caused by sinus inammation. Conversely, a tooth can refer pain to the sinus.9 However, usually the offending tooth is symptomatic or at least manifests a radiolucency that is indicative that the endodontic result is less than ideal.10 In this regard, it was considered that the teeth subjacent to the sinus might be causing the pain. It was perplexing that the teeth never demonstrated any signs or symptoms of pathosis after her occlusal equilibration. In general, an asymptomatic endodontically treated tooth that appears normal on a periapical radiograph usually indicates endodontic treatment was successful. However, there are reports that even if a periapical area seems resolved on a radiograph, microorganisms may persist indenitely11 and an inammatory process could be associated with endodontically treated teeth that appear radiographically normal.5,12-15 Pertinently, others reported 30% of the buccal or lingual plate needs to be resorbed before an apical lesion appears on a radiograph.16 Therefore, it is possible that the pain referred to the sinus area was caused by an undetectable lesion at the apex of the premolars; and there was stimulation of peripheral and central nociceptors by doloric substances, such as bradykinin, prostaglandins, leukotrienes, histamines, and so forth.17 Initiation of her pain may have been precipitated by the sinus membrane elevation over the second premolar, which compromised the tooths vascular supply, or possibly an apical lesion was irritated by instrumentation. These are hypothetical explanations, and there is no way to precisely identify the precipitating factor that resulted in the patient developing pain 2 weeks after completion of the sinus lift. Nevertheless, the literature was searched to ascertain if additional factors should be considered when confronted with a situation similar to the one presented in this case report. Several perspectives were investigated: prevalence of maxillary roots in the sinus, vascularity of endodontically treated teeth, and regional alterations of vascularity associated with sinus lifts. Roots of maxillary molars or premolars can protrude into the sinus cavity, but this occurs less often than expected because conventional radiographs are misleading. It was reported that the sinus oor extends between adjacent teeth or between individual roots in about half of the population.18 However, it has been histologically demonstrated that most roots that appear radiographically to protrude into the sinus are surrounded by a thin layer of cortical bone and this bone is perforated 14% to 28% of the time.19 Furthermore, when panoramic lms and CT scans were compared, only 39% of subjects manifesting roots

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projecting into sinus in panoramic radiographs showed protrusion on CT images.20 These ndings conrm that apices of teeth may be exposed when the sinus membrane is elevated. The blood supply to teeth is derived from three sources: 1) periodontal ligament, 2) periosteum, and 3) endosteal vessels.21 If endodontics are performed, the tooth remains embedded in a highly vascular periodontal ligament22 and blood supply at the apex is similar to a vital tooth.23 Likewise, healing is associated with the formation of new blood vessels if a tooth had a successful apicoectomy.24 No data were located that indicated endodontically treated teeth have compromised apical vascularity, thereby making them more susceptible to failure than vital teeth. There are vascular changes in the bone preceding a sinus lift. Investigators noted that the maxilla is densely vascularized in dentate subjects;25,26 however, the blood supply is permanently reduced (diameter and number of vessels decrease) with aging and atrophy of bone after tooth removal.27 Eventually, the antral oor can be diminished to a thin layer of compact bone.28,29 Because thin bone cannot be supplied with centromedullary vessels, it may only be supplied periosteally.30 Furthermore, it is possible at locations along the sinus oor that there is no bone or blood vessels.31 Therefore, it seems that reduction of subantral bone is associated with alterations of blood supply to the oor of the sinus. With respect to blood supply to the sinus region, there are three primary blood vessels: 1) the posterior lateral nasal artery, 2) the posterior superior alveolar artery, and 3) the infraorbital artery.30,32 The latter two form intraosseous and extraosseous anastomoses in the lateral antral wall and provide vascularity to the schneiderian membrane.30 These blood vessels may be transected during creation of the lateral window, thereby decreasing blood supply to the region.33 Furthermore, Traxler et al.33 indicated that the periosteum should be separated with great care to prevent damage to extraosseous anastomoses. In this regard, it has been suggested that when elevating the schneiderian membrane, if teeth protrude into the sinus it is possible to devitalize them.34 Theoretically, this could occur by severing the nerve or vascular supply at the apex. However, no studies were found that addressed this issue. The last enigma related to this case is referred pain, which can be a perplexing problem. It may lead to inappropriate dental care if the origin of pain is not found.35 Pertinently, the lack of signs indicating a sinus infection dictated not to remove the sinus graft. Similarly, failure to detect signs suggesting that the premolars were the source of her pain precluded, reaching the conclusion that teeth #4 and #5 should

be removed. The dilemma was that the patient had intermittent pain that she believed was originating in her sinus, and it had not resolved despite several courses of antibiotics. A CT scan was ordered 5 weeks after she became symptomatic. In retrospect, the CT scan could have been obtained sooner to rule out the possibility of a sinus infection because this determination could not be made based solely on clinical ndings. Discussion was initiated regarding removal of asymptomatic teeth (#4 and #5) once the CT scan demonstrated a well-contained sinus graft and a clear sinus. There was a concern that the teeth could be removed, and if the pain persisted another predicament would have been created. The decision was made to proceed with extraction of asymptomatic teeth and to maintain the sinus graft. When the teeth were extracted the apices of the teeth were examined, and the gutta percha did not protrude past the root apices. As indicated, her relief was postponed because of development of a local osteitis at site #4. There was no apparent reason for development of a local osteitis, and when it resolved the patient was comfortable. CONCLUSIONS In retrospect, numerous times the decision to remove the sinus graft seemed more logical than removal of asymptomatic premolars. However, failure to validate the presence of a sinus infection and reluctance to remove the sinus graft was a motivation not to give into expediency. It is unknown why the premolars became exacerbated subsequent to the sinus lift procedure. Hypothetically, membrane elevation over tooth #4 or the initial occlusal trauma may have precipitated a sequence of biochemical or bacterial events that resulted in referred pain, while the premolars remained asymptomatic. Ultimately, the patient was very pleased that the sinus graft was not removed because its presence will facilitate her receiving dental implants at sites #3 and #4 and a xed prosthesis to include her rst molar. ACKNOWLEDGMENT The authors report no conicts of interest related to this case report. REFERENCES
1. Raja SV. Management of the posterior maxilla with sinus lift: Review of techniques. J Oral Maxillofac Surg 2009;67:1730-1734. 2. Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impact on implant survival. J Periodontol 2004;75:511-516. 3. Ailor JE Jr. Managing incomplete tooth fractures. J Am Dent Assoc 2000;131:1168-1174. 781

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4. Christensen GJ. The cracked tooth syndrome: A pragmatic treatment approach. J Am Dent Assoc 1993; 124:107-108. 5. Tataryn RW. Rhinosinusitis and endodontic disease. In: Ingle JI, Balkind LK, Baumgartner JC, eds. Ingles Endodontics, 6th ed. Hamilton, Ontario: BC Decker; 2008:626-637. 6. Pashley DH, Walton RE, Slavkin HC. Histology and physiology of the dental pulp. In: Ingle JI, Balkind LK, Baumgartner JC, eds. Ingles Endodontics, 6th ed. Hamilton, Ontario: BC Decker; 2008:25-62. 7. Sawaya RA. Trigeminal neuralgia associated with sinusitis. ORL J Otorhinolaryngol Relat Spec 2000; 62:160-163. 8. Okeson JP, Falace DA. Nonodontogenic toothache. Dent Clin North Am 1997;41:367-383. 9. Rotstein I, Simon HS. Endodontic-periodontal interrelationships. In: Ingle JI, Balkind LK, Baumgartner JC, eds. Ingles Endodontics, 6th ed. Hamilton, Ontario: BC Decker; 2008;638-659. 10. Ehrmann EH. The diagnosis of referred orofacial dental pain. Aust Endod J 2002;28:75-81. 11. Brynolf I. A histological and roentgenological study of the peri-apical region of upper incisors. Odontol Revy 1967;18(Suppl. 11):1-176. 12. Green TL, Walton RE, Taylor JK, Merrell P. Radiographic and histologic periapical ndings of root canal treated teeth in cadaver. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;83:707-711. 13. Seltzer S. Long-term radiographic and histological observations of endodontically treated teeth. J Endod 1999;25:818-822. 14. Rowe AH, Binnie WH. Correlation between radiological and histological inammatory changes following root canal treatment. J Br Endod Soc 1974;2:57-63. 15. Lin LM, Skribner JE, Gaengler P. Factors associated with endodontic treatment failures. J Endod 1992; 18:625-627. 16. Ortman LF, McHenry K, Hausmann E. Relationship between alveolar bone measured by 125I absorptiometry with analysis of standardized radiographs: 2. Bjorn technique. J Periodontol 1982;53:311-314. 17. Jacinto RC, Gomes BP, Shah HN, Ferraz CC, Zaia AA, Souza-Filho FJ. Quantication of endotoxins in necrotic root canals from symptomatic and asymptomatic teeth. J Med Microbiol 2005;54:777-783. 18. Hauman CH, Chandler NP, Tong DC. Endodontic implications of the maxillary sinus: A review. Int Endod J 2002;35:127-141. 19. Wehrbein H, Diedrich P. The initial morphological state in the basally pneumatized maxillary sinus: A radiological-histological study in man (in German). Fortschr Kieferorthop 1992;53:254-262. 20. Sharan A, Madjar D. Correlation between maxillary sinus oor topography and related root position of posterior teeth using panoramic and cross-sectional computed tomography imaging. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006;102:375-381.

21. Nobuto T, Imai H, Suwa F, et al. Microvascular response in the periodontal ligament following mucoperiosteal ap surgery. J Periodontol 2003;74:521528. 22. Gutman JL. History of endodontics. In: Ingle JI, Balkind LK, Baumgartner JC, eds. Ingles Endodontics, 6th ed. Hamilton, Ontario: BC Decker; 2008:43. 23. Huettner RJ, Young RW. The movability of vital and devitalized teeth in the Macacus rhesus monkey. Oral Surg Oral Med Oral Pathol 1955;8:189-197. 24. Lin LM, Di Fiore PM, Lin J, Rosenberg PA. Histological study of periradicular tissue responses to uninfected and infected devitalized pulps in dogs. J Endod 2006;32:34-38. 25. Marx RE. Clinical application of bone biology to mandibular and maxillary reconstruction. Clin Plast Surg 1994;21:377-392. 26. Bell WH, You ZH, Finn RA, Fields RT. Wound healing after multisegmental Le Fort I osteotomy and transection of the descending palatine vessels. J Oral Maxillofac Surg 1995;53:1425-1433; discussion 14331434. 27. Soikkonen K, Wolf J, Hietanen J, Mattila K. Three main arteries of the face and their tortuosity. Br J Oral Maxillofac Surg 1991;29:395-398. 28. Watzek G, Solar P, Ulm C, Matejka M. Surgical criteria for endosseous implant placement: An overview. Pract Periodontics Aesthet Dent 1993;5:87-94; quiz 96. 29. Ulm CW, Solar P, Gsellmann B, Matejka M, Watzek G. The edentulous maxillary alveolar process in the region of the maxillary sinus: A study of physical dimension. Int J Oral Maxillofac Surg 1995;24:279-282. 30. Solar P, Geyerhofer U, Traxler H, Windisch A, Ulm C, Watzek G. Blood supply to the maxillary sinus relevant to sinus oor elevation procedures. Clin Oral Implants Res 1999;10:34-44. 31. Selden HS. The interrelationship between the maxillary sinus and endodontics. Oral Surg Oral Med Oral Pathol 1974;38:623-629. 32. Norton NS, ed. Netters Head and Neck Anatomy for Dentistry. Philadelphia: WB Saunders; 2007:299301. 33. Traxler H, Windisch A, Geyerhofer U, et al. Arterial blood supply of the maxillary sinus. Clin Anat 1999; 12:417-421. 34. van den Bergh JP, ten Bruggenkate CM, Disch FJ, Tuinzing DB. Anatomical aspects of sinus oor elevations. Clin Oral Implants Res 2000;11:256-265. 35. Falace DA, Reid K, Rayens MK. The inuence of deep (odontogenic) pain intensity, quality, and duration on the incidence and characteristics of referred orofacial pain. J Orofac Pain 1996;10:232-239. Correspondence: Gary Greenstein, 900 West Main St., Freehold, NJ 07728. Fax: 732/780-7798; e-mail: ggperio@ aol.com. Submitted November 16, 2009; accepted for publication January 9, 2010.

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