Closure of 1.

5-cm Alveolar Oral Antral Fistula with

Intra-alveolar Sinus Membrane Elevation and Bone
Morphogenetic Protein-2/Collagen Graft Followed by
Dental Implant Restoration: Case Report
Jared R. Cottam, DDS, MD1/Ole T. Jensen, DDS, MS2/Lucas Beatty, DDS, MD1/Jason Ringeman, DDS, MD3

Closure of a 1.5-cm oral antral fistula was done in combination with sinus floor and extraction
socket grafting using recombinant human bone morphogenetic protein-2 within a collagen
sponge matrix. The approach to the sinus was transalveolar, with elevation of the sinus
membrane done through a molar extraction socket. Following graft placement, soft tissue
repair was done with a buccal advancement flap. A dental implant was subsequently placed
and restored. Peri-implant bone and implant stability were well maintained at the 1-year follow
up examination. Int J Oral Maxillofac Implants 2013;28:e277–e282. doi: 10.11607/jomi.te08

Key words: bone morphogenetic protein-2, combined socket–sinus floor repair, extraction
socket augmentation, intra-alveolar sinus fistula repair, oral antral fistula, sinus bone graft

C
losures of oral antral fistulae that are 1 cm or
larger have been accomplished with various
methods, including the use of local soft tissue
flaps1–5 or distant site soft tissue flaps such as tongue
flaps,6–8 the use of a buccal fat pad,9,10 application of
alloplastic materials such as gold foil,11,12 bone graft-
ing,13–15 local osteotomies,16 vascularized flaps,17 and
even placement of a dental implant.18 The exact loca-
tion of the fistula—palatal or buccal, posterior or rela-
tively anterior, involving the antrum only or combined
with the nasal cavity—can guide the clinician toward
a specific technique.19–21 When the fistula is located
intra-alveolarly, a situation that is most often caused
by a dental extraction or loss of a dental implant, and
1Private
practice, Seattle, Washington, USA.
2Private practice in oral surgery, Denver, Colorado, USA.
3 Fellow, Tissue Engineering Institute of Colorado, Denver,
Colorado, USA.
Correspondence to: Dr Jared R. Cottam, 15515 3rd Ave SW,
Suite E, Burien, WA 98166, USA. Email:jamcottam@hotmail.com
©2013 by Quintessence Publishing Co Inc.
if there is still some residual alveolar height, an intra-
socket approach can be attempted.22 Intrasocket pro-
cedures work well when the communication is small,
perhaps less than 5 mm,22 but when the sinus floor
defect is large (ie, 10 mm or larger), intrasocket repair
becomes more challenging. One reason for this may
be that the exposed root surfaces of adjacent teeth
and/or periodontal disease of adjacent teeth hamper
repair potential.23,24
Another consideration is restoration of the bone
defect. Most clinicians favor repairing the fistula first,
following this later with alveolar bone grafting13,25;
however, the tibial autograft has been used for com-
bined sinus grafting and fistula repair.15
Reported here is the treatment of a patient who re-
ceived combined oral antral fistula repair and grafting
of a maxillary first molar site. The entire sinus floor had
been lost following dental extraction, leaving a 1-cm
fistula that had not closed after 8 months. The treat-
ment involved sinus membrane elevation, grafting with
recombinant human bone morphogenetic protein-2
(rhBMP-2) (1.5 mg/mL) within a collagen sponge
matrix, and primary closure using a Burger flap ad-
vanced from the vestibule in conjunction with a palatal
rotation flap to obtain tension-free primary closure.26
Intra-alveolar sinus membrane elevation was done to
facilitate placement of the BMP-2/collagen graft.27

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 Cottam et al
Fig 1   A 52-year-old man presented at 8 months after extraction
of a maxillary first molar; the site subsequently developed a 1-cm
(soft tissue) oral antral fistula.
Fig 3  Exposure of the fistula site is done laterally, revealing a
1.5- × 1.2-mm osseous defect that communicates with the maxil-
lary sinus.
Case Report
A 52-year-old man presented with an oral antral fistula
in the maxillary right first molar area that measured 1 cm
in diameter (soft tissue). The patient had undergone
dental extraction at another clinic 8 months previously.
He had received several courses of antibiotics for sinus
infection but no surgical attempts had been made to
close the defect (Fig 1). The patient presented in no
acute distress but with symptoms of chronic sinusitis.
Exudate drained from the maxillary right first molar site,
where a large sinus communication was evident (Fig 2).
A screening computed tomographic scan revealed a
clouded sinus.
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Fig 2  A pretreatment computed tomo-
graphic scan shows the oral antral com-
munication and occlusion of the entire
right maxillary sinus.
Fig 4  Following elevation of the sinus membrane and place-
ment of a collagen patch over the membrane perforation, BMP-2/
collagen sponge is used to graft the sinus floor and extraction
socket.
The patient was prescribed antibiotics in conjunc-
tion with aggressive sinus hygiene, which cleared the
sinus after 3 weeks. The ostium appeared patent.
The patient then underwent a surgical procedure in
which a fistulectomy was performed, the bony defect was
exposed, and the sinus was flushed of mucus and other
debris with normal saline. The osseous defect measured
1.5 × 1.2 cm (Fig 3). An intra-alveolar approach was then
used to elevate the sinus membrane circumferentially. This
reduced the diameter of the sinus membrane perforation,
as the membrane folded in upon itself. The perforation
was then patched with a resorbable collagen mem-
brane placed within the sinus cavity. BMP-2 within a
collagen sponge carrier (Infuse, Medtronic) was frag-

Fig 5   Six months later, the sinus is clear
and bone consolidation is apparent.
Fig 6  The consolidated sinus floor and
socket graft are confluent with type II to III
bone.46
mented and placed in layers to occlude the bony defect
as well as serve as grafting material for the sinus floor
(Fig 4). Tension-free primary closure was obtained by
using a split-thickness palatal rotation flap based on the
greater palatine artery in conjunction with a Burger buc-
cal advancement flap based on the posterior maxillary
vasculature. The two flaps provided double closure of the
defect: the palatal flap was placed first, and the buccal
advancement flap was sewed over the top following de-
nudation of the epithelial layer of the deeper flap.
After 6 months, a computed tomographic scan indi-
cated a clear sinus (Fig 5), with good bone consolida-
tion in both the sinus floor and alveolus (Fig 6). Following
administration of local anesthesia, through a crestal inci-
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NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
Cottam et al
Fig 7  One year later, the implant restoration shows favorable
marginal bone levels and functional osseointegration.
sion, the site was then exposed. There was no evidence
of the residual defect; only natural bone was apparent. A
wide-body implant (9 × 9 mm, Southern Implants) was
placed with an insertion torque greater than 50 Ncm us-
ing a one-stage technique with placement of a healing
screw. After 4 months, the implant was restored with a
single crown. At the 1-year follow up examination, the
implant was found to be in functional occlusion. A peri-
apical radiograph showed that the peri-implant bone had
been maintained (Fig 7).
The International Journal of Oral & Maxillofacial Implants e279
 Cottam et al

Collagen membrane
Sinus
BMP-2 graft

Bacterial infection

Mucus-filled sinus membrane

Single capillary New bone matrix de-

sprout posited by osteoblasts
Osteoblast
lining

a
Fig 8a   A large alveolar defect that communicates with the sinus
cavity leads to chronic sinusitis. Osteoclasts with
Osteocyte microvilli-ruffled
Fig 8b  Following sinus membrane elevation and patching of membrane
the membrane perforation with collagen tape, a BMP-2 collagen excavating through
calcified matrix to
sponge graft can be placed in the sinus floor and extraction socket. Bone graft mixed with new remodel bone
b organic bone matrix

Discussion in a relatively sterile environment, in contrast to treat-

The use of BMP-2 in a setting of chronic oral antral
communication following fistulectomy and sinus mem-
brane elevation is well within the parameters of the
US Food and Drug Administration–approved use of
this morphogen.28 BMP-2 consistently forms bone in
the sinus floor, even when there are large perforations
present following membrane reflection.28 In addition,
BMP-2 has been studied and is approved for use in
extraction socket bone grafting and was found to re-
form buccal and palatal walls and fill extraction site
wounds with viable bone.29–31
The present defect, then, was a combined site that
was amenable to treatment using BMP-2/ACS (Fig
8a). Bone fill in this setting was consistent with the
outcome following posterior maxillary alveolar split os-
teotomy combined with sinus floor grafting; the latter
technique has been shown to work well but is done
ment of a long-standing oral antral communication.32
Stem cells that may convert to bone-forming cells
issue from the socket bone walls, the periosteum, the
periosteal vasculature, and the sinus membrane itself
(Fig 8b).33–37 Signal-enhanced grafting provides a
way for localized as well as distant cell migration to
the wound site to form bone as well as the supporting
vasculature and associated soft tissues (Fig 8c).38–41
This de novo bone is of such high quality that it can
support an implant on its own; no “native” bone is re-
quired for primary fixation or eventual osseointegration
(Fig 8d).42
One other consideration for the use of BMP in rela-
tively infected sites is its apparent suppression of in-
fection in the grafting setting.43 Whereas the use of
autogenous marrow or even a bone substitute may be
considered, there is probably a greater risk of infection
using osteoconductive agents than with the use of

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 Cottam et al

Bone remodeling
from graft Bone remodeling
from graft

Bone remodeling
from graft

Dental
New bone implant
Epithelial
proliferation

Basal
lamina

d
Fig 8c   Stem cell sources for healing this defect come from bone,
periosteum, perivascular tissues, sinus membrane, and the blood-
stream by inductive signaling from the BMP-2 graft site, causing
new bone to form.

Fig 8d  Implant placement in large defects (ie, 1 cm or larger)

c should commence approximately 6 months after BMP-2 graft
placement.

BMP-2 alone, as the incidence of infection of BMP-2  
sinus or socket grafts is considerably lower.40–42 This
has been demonstrated in animal studies, where heal-  
ing occurred in infected sites treated with BMP-2.
The mechanism for this is unclear but may be related
to increased mRNA expression of bone formation
genes.44  
Other issues to consider when using a combined
repair technique are the need to be certain of a patent  
ostium as well as an uninfected sinus prior to under-
taking surgical closure.1,45  
 
References
  1. Yalçın S, Oncü B, Emes Y, Atalay B, AktaşI. Surgical treat-  
ment of oroantral fistulas: A clinical study of 23 cases. J Oral
Maxillofac Surg 2011;69:333–339.
2. Visscher SH, van Minnen B, Bos RR. Closure of oroantral
communications: A review of the literature. J Oral Maxillofac
Surg 2010;68:1384–1391.
3. Anavi Y, Gal G, Silfen R, Calderon S. Palatal rotation-ad-
vancement flap for delayed repair of oroantral fistula:
A retrospective evaluation of 63 cases. Oral Surg Oral Med
Oral Pathol Oral Radiol Endod 2003;96:527–534.
4. Dergin G, Gurler G, Gursoy B. Modified connective tissue
flap: A new approach to closure of an oroantral fistula. Br J
Oral Maxillofac Surg 2007;45:251–252.
5. Awang MN. Closure of oroantral fistula [review]. Int J Oral
Maxillofac Surg 1988;17:110–115.
6. Al-Qattan MM. A modified technique of using the tongue tip
for closure of large anterior palatal fistula. Ann Plast Surg
2001;47:458–460.
7. Sachs SA, Kay SA, Specter J, Stern M. Treatment of a persis-
tent oro-antral fistula with a posteriorly based lateral tongue
flap. Int J Oral Surg 1979;8:225–228.
8. Siegel EB, Bechtold W, Sherman PM, Stoopack JC. Pedicle
tongue flap for closure of an oroantral defect after partial
maxillectomy. J Oral Surg 1977;35:746–748.

The International Journal of Oral & Maxillofacial Implants e281

© 2013 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
 Cottam et al
  9. Singh J, Prasad K, Lalitha RM, Ranganath K. Buccal pad
of fat and its applications in oral and maxillofacial surgery:
A review of published literature (February) 2004 to (July)
2009. Oral Surg Oral Med Oral Pathol Oral Radiol Endod
2010;110:698–705.
10. Poeschl PW, Baumann A, Russmueller G, Poeschl E, Klug C,
Ewers R. Closure of oroantral communications with Bichat’s
buccal fat pad. J Oral Maxillofac Surg 2009;67:1460–1466.
11. Steiner M, Gould AR, Madion DC, Abraham MS, Loeser JG.
Metal plates and foils for closure of oroantral fistulae. J Oral
Maxillofac Surg 2008;66:1551–1555.
12. Visscher SH, van Minnen B, Bos RR. Closure of oroantral
communications using biodegradable polyurethane foam: A
feasibility study. J Oral Maxillofac Surg 2010;68:281–286.
13. Watzak G, Tepper G, Zechner W, Monov G, Busenlechner
D, Watzek G. Bony press-fit closure of oro-antral fistulas: A
technique for pre-sinus lift repair and secondary closure.
J Oral Maxillofac Surg 2005;63:1288–1294.
14. Nadal E, Sabás M, Dogliotti P, Espósito R. Secondary alveo-
lar bone grafting: Our experience with olecranon bone graft.
J Craniofac Surg 2010;21:371–374.
15. Jensen OT. Sinus bone grafting for oral antral fistulae [com-
ment]. Oral Surg Oral Med Oral Pathol Oral Radiol Endod
2004;97:4.
16. Deune EG, Manson PN. Use of the serratus anterior free
flap to treat a recurrent oroantral fistula. J Craniofac Surg
2004;15:335–340.
17. Lazaridis N, Tilaveridis I, Venetis G, Lazaridou M. Maxillary sinus
osteoplasty with vascularized pedicled bone flap. Oral Surg
Oral Med Oral Pathol Oral Radiol Endod 2008;106:828–832.
18. Doobrow JH, Leite RS, Hirsch HZ. Concomitant oroantral
communication repair and immediate implant placement:
A five-year case report. Implant Dent 2008;17:176–181.
19. Güven O. A clinical study on oroantral fistulae. J Craniomaxil-
lofac Surg 1998;26:267–271.
20. Abuabara A, Cortez AL, Passeri LA, de Moraes M, Moreira
RW. Evaluation of different treatments for oroantral/oronasal
communications: Experience of 112 cases. Int J Oral Maxil-
lofac Surg 2006;35:155–158.
21. Punwutikorn J, Waikakul A, Pairuchvej V. Clinically significant
oroantral communications—A study of incidence and site. Int
J Oral Maxillofac Surg 1994;23:19–21.
22. Hernando J, Gallego L, Junquera L, Villarreal P. Oroantral
communications. A retrospective analysis. Med Oral Patol
Oral Cir Bucal 2010;15:e499–e503.
23. Felix DH, Wray D, Smith GL, Jones GA. Oro-antral fistula: An
unusual complication of HIV-associated periodontal disease.
Br Dent J 1991;171:61–62.
24. Yilmaz T, Suslu AE, Gursel B. Treatment of oroantral fistula: Ex-
perience with 27 cases. Am J Otolaryngol 2003;24:221–223.
25. Gacic B, Todorovic L, Kokovic V, et al. The closure of oroantral
communications with resorbable PLGA-coated beta-TCP root
analogs, hemostatic gauze, or buccal flaps: A prospective
study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod
2009;108:844–850.
26. Lee BK. One-stage operation of large oroantral fistula clo-
sure, sinus lifting, and autogenous bone grafting for dental
implant installation. Oral Surg Oral Med Oral Pathol Oral
Radiol Endod 2008;105:707–713.
27. Velich N, Németh Z, Tóth C, Szabó G. Long-term results with
different bone substitutes used for sinus floor elevation.
J Craniofac Surg 2004;15:38–41.
28. Boyne PJ, Lilly LC, Marx RE, et al. De novo bone induc-
tion by recombinant human bone morphogenetic protein-2
(rhBMP-2) in maxillary sinus floor augmentation. J Oral Maxil-
lofac Surg 2005;63:1693–1707.
e282 Volume 28, Number 5, 2013
© 2013 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.
NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
29. Fiorellini JP, Howell TH, Cochran D, et al. Randomized study
evaluating recombinant human bone morphogenetic protein-2
for extraction socket augmentation. J Periodontol 2005;76:
605–613.
30. Casado PL, Duarte ME, Carvalho W, Esmeraldo da Silva L,
Barboza EP. Ridge bone maintenance in human after extrac-
tion. Implant Dent 2010;19:314–322.
31. Howell TH, Fiorellini J, Jones A, et al. A feasibility study evalu-
ating rhBMP-2/absorbable collagen sponge device for local
alveolar ridge preservation or augmentation. Int J Periodontics
Restorative Dent 1997;17:124–139.
32. González-García R, Monje F, Moreno C. Alveolar split oste-
otomy for the treatment of the severe narrow ridge maxillary
atrophy: A modified technique. Int J Oral Maxillofac Surg
2011;40:57–64.
33. Melcher AH. Wound healing in monkey (Macaca irus) man-
dible: Effect of elevating periosteum on formation of sub-
periosteal callus. Arch Oral Biol 1971;16:461–464.
34. Rickert D, Sauerbier S, Nagursky H, Menne D, Vissink A,
Raghoebar GM. Maxillary sinus floor elevation with bovine
bone mineral combined with either autogenous bone or au-
togenous stem cells: A prospective randomized clinical trial.
Clin Oral Implants Res 2010 Sep 10 [Epub ahead of print].
35. Srouji S, Ben-David D, Lotan R, Riminucci M, Livne E, Bianco P.
The innate osteogenic potential of the maxillary sinus (Schnei-
derian) membrane: An ectopic tissue transplant model simulat-
ing sinus lifting. Int J Oral Maxillofac Surg 2010;39:793–801.
36. Kim SW, Lee IK, Yun KI, Kim CH, Park JU. Adult stem cells
derived from human maxillary sinus membrane and their os-
teogenic differentiation. Int J Oral Maxillofac Implants 2009;
24:991–998.
37. Chadipiralla K, Yochim JM, Bahuleyan B, et al. Osteogenic
differentiation of stem cells derived from human periodontal
ligaments and pulp of human exfoliated deciduous teeth. Cell
Tissue Res 2010;340:323–333.
38. Suzuki Y, Ohga N, Morishita Y, Hida K, Miyazono K, Watabe
T. BMP-9 induces proliferation of multiple types of endothelial
cells in vitro and in vivo. J Cell Sci 2010;123:1684–1692.
39. Chen D, Zhao M, Mundy GR. Bone morphogenetic proteins.
Growth Factors 2004;22:233–241.
40. Suzuki Y, Montagne K, Nishihara A, Watabe T, Miyazono K.
BMPs promote proliferation and migration of endothelial cells
via stimulation of VEGF-A/VEGFR2 and angiopoietin-1/Tie2
signalling. J Biochem 2008;143:199–206.
41. Doll B, Sfeir C, Winn S, Huard J, Hollinger J. Critical aspects
of tissue-engineered therapy for bone regeneration. Crit Rev
Eukaryot Gene Expr 2001;11:173–198.
42. Boyne PJ. Application of bone morphogenetic proteins in the
treatment of clinical oral and maxillofacial osseous defects.
J Bone Joint Surg Am 2001;83A(suppl 1):S146–S150.
43. Miller CP, Simpson AK, Whang PG, et al. Effects of recom-
binant human bone morphogenetic protein 2 on surgical
infections in a rabbit posterolateral lumbar fusion model.
Am J Orthop 2009;38:578–584.
44. Brick KE, Chen X, Lohr J, Schmidt AH, Kidder LS, Lew WD.
rhBMP-2 modulation of gene expression in infected segmental
bone defects. Clin Orthop Relat Res 2009;467:3096–3103.
45. Anzalone JV, Vastardis S. Oroantral communication as an os-
teotome sinus elevation complication. J Oral Implantol 2010;
36:231–237.
46. Lekholm U, Zarb GA. Patient selection and preparation.
In: Branemark P-I, Zarb GA, Albrektsson T (eds). Tissue-
Integrated Prostheses: Osseointegration in Clinical Dentistry.
Chicago: Quintessence, 1985:199–209.