ORIGINAL ARTICLE
Autogenous Bone Grafts Contamination After Exposure to the Oral Cavity Hugo Nary Filho, PhD,* Tábata Fernandes Pinto,† Caio Peixoto de Freitas,* Paulo Domingos Ribeiro-Junior, PhD,* Pâmela Letícia dos Santos, PhD,* and Mariza Akemi Matsumoto, PhD* Abstract: The purpose of this paper was to analyze specimens of autogenous bone block grafts exposed to the oral cavity after ridge reconstructions. Specimens of chronic suppurative osteomyelitis (CSO) of the jaws were used as comparison for bacterial colonization pattern. For this, 5 specimens of infected autogenous bone grafts were used and 10 specimens of CSO embedded in paraffin were stained with Brown and Brenn technique and analyzed under light microscopy. The results showed a similar colonization pattern in both situations, with the establishment of bacterial biofilm and the predominance of Gram-positive bacteria. The conclusion was that the similarity in bacterial distribution and colonization between autogenous bone grafts and CSO stresses the necessity of more invasive procedures for the treatment of the autogenous bone grafts early exposed to the oral cavity. Key Words: Bone reconstruction, autogenous bone graft, bacterial biofilm, osteomyelitis (J Craniofac Surg 2014;25: 412–414)
T
ooth loss is followed by important changes and remodeling of alveolar ridge, eventually making the rehabilitation with endosseous implants extremely difficult due to the remaining width and height bone volume.1 In face of these situations, literature provide a number of options for the reconstruction of atrophic ridges, among them the use of autogenous, homogenous, and heterogeneous bone grafts, along with the alloplastic implants.2 Autogenous bone graft is considered the first option due to its favorable properties, extensively described elsewhere3 resulting in better postoperative conditions and avoiding immunological
What Is This Box? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code links to the online version of the article.
From the *Department of Oral Biology Post Graduation, and †Dentistry Course, University do Sagrado Coração (USC), Bauru, São Paulo, Brazil. Received December 1, 2013. Accepted for publication December 28, 2013. Address correspondence and reprint requests to Mariza Akemi Matsumoto, PhD, Departament of Pró-Reitoria de Pesquisa e Pós-graduação, Universidade Sagrado Coração, Rua Irmã Arminda, 10-50, 17011-160 Bauru, SP, Brazil; E-mail: [email protected] The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000682
412
incompatibilities.4,5 However, this kind of graft presents some limitations such as donor-site morbidity, increased surgical time, and limited available bone.6 Complications at the recipient area also occur, mainly related to contamination of the graft due to its early exposure usually resulting in failure of the procedure.7 Although it represents a complication that most of the reconstructive oral surgeons have already, or will, faced in their clinical practice, only a few reports are cited in literature.8,9 One of the most important infectious diseases of the bones, including the jaws, is osteomyelitis caused by the installation of bacterial biofilm in the medullary space that can spread to the periosteum, cortical bone, and soft tissues.10 Its classification in acute or chronic suppurative osteomyelitis (CSO) is dependent upon the duration of the disease.11 Sequestrectomy of the necrotic tissue and debridement of the surrounding bone and systemic antibiotic therapy is the treatment of choice, sometimes associated to hyperbaric oxygen therapy.12 Staphylococci are considered the most infecting microorganisms of bone tissue13–15 being the species aureus the most commonly found. In an in vitro study, Sanchez et al (2013)16 observed the behavior of osteoblastic cells in Staphylococcus aureus biofilm conditioned media and revealed a reduced osteoblast differentiation and viability, along with an increase in apoptosis with an up-regulated expression of the receptor activator of nuclear factor kappa-B ligand, responsible for recruitment and activation of the osteoclasts. In an interesting study, Clauss et al (2010)17 compared early and mature S. aureus biofilm formation on the surface of fresh and fresh-frozen human bone grafts from femoral heads, and processed human and bovine bone grafts, finding a decreased biofilm density on fresh and fresh-frozen grafts after 24 hours. Although minimal structural architectural differences were found among the materials, biological characteristics seemed to be relevant, as the maintenance of serum proteins and the presence of bone marrow content on fresh grafts’ surface, which are lost in the processed bones. In this way, similarities regarding the microorganism and evolution of bone infection caused by the installation of the biofilms are evident. In this way, the present study aimed to analyze the histological pattern of mature biofilm in early exposed bone grafts and to compare them with CSO, in an attempt to guide clinicians to a more appropriate resolution.
MATERIALS AND METHODS Samples from 5 patients who underwent horizontal alveolar reconstruction (onlay) with autogenous bone grafts retrieved from the mandibular ramus (Table 1) were obtained. All the patients presented early exposure of the block grafts due to suture dehiscence, up to 1 month after the reconstructive procedure, which were immediately removed and prepared for a further reconstruction procedure. The removed blocks were fixed in 10% buffered formalin and decalcified in 4% EDTA, to be processed under histologic routine technique, sectioned in their longer axis and stained with Brown and Brenn to
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Autogenous Bone Grafts Contamination
TABLE 1. Characterization of the Patients Submitted to Autogenous Bone Grafts Alveolar Ridge Reconstruction Patient
Gender
Age
Donor Site
Receptor Site
1
Male Male Male Male Female
Non-informed 44 63 68 71
Mandibular symphysis Iliac crest Mandibular body and angle Iliac crest Iliac crest
Mandible Mandible Mandible Mandible Mandible
2 3 4 5
evidence Gram-positive and Gram-negative bacteria. The slices were analyzed under light microscopy for morphological characterization of the grafts. In the same way, and for comparative purposes, CSO paraffin-embedded specimens were selected from the archives of Oral Pathology Laboratory from the Sagrado Coração University (Bauru, SP, Brazil) that also could be clinically characterized. These specimens were re-sectioned and stained by the same technique of the bone grafts, used as a parameter for the microscopic analysis.
RESULTS Autogenous Bone Block Grafts In the specimens of autogenous bone grafts fragments (Fig. 1), nonviable bone were present, with no signs of bone formation or remodeling. Bone surfaces were irregular, probably due to previous osteoclastic activity. Organized bacterial biofilms attached on bone surface were constituted predominantly of Gram-positive bacteria, stained in purple. However, eventual osteocytes lacunas were filled by Gram-negative bacteria, stained in red (Fig. 2A–C).
CSO CSO specimens revealed nonviable bone tissue, characterized by the absence of osteoblasts, lining cells, and osteocytes in bone matrix. No evidence of remodeling or bone formation was noted. Bone surface was irregular and covered by bacterial biofilms with the predominance of Gram-positive bacteria, stained in purple. Biofilms could be visualized filling bone lacunae and Havers channels. Intense mononuclear and neutrophilic infiltrate was observed in medullar spaces (Fig. 3A–C).
FIGURE 1. Autogenous onlay bone graft retrieved after contamination and exposure.
FIGURE 2. Autogenous bone grafts—A, nonviable bone fragments (B) showing irregular surface covered by Gram-positive bacterial biofilm (arrows); B, well-established Gram-positive biofilm covering bone surfaces (arrows); C, Gram-negative biofilms could be seen filling some bone lacunas (small arrows) (Brown and Brenn; bars = 100 μm).
DISCUSSION Autogenous bone grafts are still considered the gold standard for functional and aesthetic reconstructions of atrophic alveolar ridges in implantology18,19; however, this procedure can lead to transoperative and postoperative complications, the last one being more frequent and associated to graft failure. Some of them are reported in literature, as presented by Schwartz-Arad and Levin (2005)8 in an analysis involving 10 patients who underwent extensive maxillary reconstructions using intraoral block bone grafts resulting in 2 cases of minimal graft exposure and one partially failed, being partially removed. In another report, 64 onlay bone grafts were analyzed, with 12.5% of them considered as failure due to their exposure or removal.9 Unfortunately, a lack of details about these complications such as the time of the grafts exposure or removal, or the first therapeutic actions, make difficult to delineate a preventive or treatment protocol. The contamination and infection of exposed autogenous bone grafts in the oral cavity are understandable when one considers autogenous bone grafts as temporary foreign bodies since they are free of vascularization and present a reduced resistance against bacterial infection, as stated by Van Blitterswijk et al (1986).20 In the present study, the pattern of bacterial colonization in autogenous bone exposed to the oral cavity due to suture dehiscence was compared to
FIGURE 3. Chronic suppurative osteomyelitis—A, bone fragments showing no vitality, with absence of bone cells (B); B, bone surface covered by established biofilm predominantly constituted by Gram-positive bacteria stained in purple (arrows); C, note intense neutrophilic infiltrate in medullar spaces (*) (Brown and Brenn; bars = 100 μm).
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
413
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Filho et al
CSO. The pattern of biofilm installation can play an important role in the treatment of infectious conditions that affect bone tissue. Systemic antibiotic therapy, an even topic, can control the symptoms of the infection, but is limited in eliminating the bacteria that are attached in the biofilm. Besides, some studies have been shown that the decrease in nutrients and oxygen is a condition that transmutate some bacteria to a state of resistant phenotype, and to constitute a biofilm with genes resistant to antimicrobial drugs.21,22 For these reasons, this kind of infection frequently reappears after antibiotic therapy and is more efficiently resolved with the mechanical removal of the affected tissue.13,23,24 Although infected bone grafts and CSO constitute different pathological conditions, it is clear that bone tissue commitment is quite similar, as shown by the microscopic pattern of biofilm distribution and quality in both conditions as evidenced in this study. The predominance of Gram-positive bacteria agrees with the prevalence of the genus Staphylococci in both conditions. The presence of the biofilm in bone surface and lacunae, the mineralized matrix, and the glycocalix formation25–29 makes easy the understanding of the poor action of drugs and the necessity of surgical removal of the affected bone. The conclusion was that the similarity in bacterial distribution and colonization between exposed bone block grafts and CSO stresses the necessity of more invasive procedures for their resolution. The total removal of the compromised bone seems to be the more indicated attitude, considering the difficulty in reverting such an organized contamination in a poor vascularized tissue. ACKNOWLEDGMENTS The authors are thankful to Maira Cristina Rondina Couto for her histotechnical assistance. This work was supported by grants from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).
REFERENCES 1. Sbordone L, Toti P, Fabris GM, et al. Implant Sucess in sinus lifted maxillae and native bone: a 3-year clinical and computerized tomographic follow-up. Int J Oral Maxillofac Implants 2009;24:316–324 2. Esposito M, Grusovin MG, Felice P, et al. The efficacy of horizontal and vertical bone augmentation procedures for dental implants—a Cochrane systematic review. Eur J Oral Implantol 2009;2:167–184 3. Zouhary KJ. Bone graft harvesting from distant sites: concepts and techniques. Oral Maxillofac Surg Clin North Am 2010;22:301–316 4. Keller E, Tolman DE, Eckert S. Surgical implants for bone reconstruction of advanced maxillary commitment autogenous onlay block bone grafts and osseointegrated endosseous implants: a 12-year study of 32 consecutive patients. Int J Oral Implantes Maxillofac 1997;14:197–209 5. Cordaro L, Amade DS, Cordaro M. Clinical results of alveolar ridge augmentation with mandibular block bone grafts in partially edentulous patients prior to implant placement. Clin Oral Implants Res 2002;13:103–111 6. McAllister DR, Joyce MJ, Mann BJ, et al. Allograft update: the current status of tissue regulation, procurement, processing and sterilization. Am J Sports Med 2007;35:2148–2158 7. Bahat O, Fontanesi RV. Complications of graft in atrophic jaws edentulous or partially edentulous. Int J Periodontics Restorative Dent 2001;21:487–495
414
8. Schwartz-Arad D, Levin L. Intraoral autogenous block onlay bone grafting for extensive reconstruction of atrophic maxillary alveolar ridges. J Periodontol 2005;76:636–641 9. Schwartz-Arad D, Levin L, Sigal L. Surgical success of intraoral autogenous block onlay bone grafting for alveolar ridge augmentation. Implant Dent 2005;14:131–138 10. Koorbusch GF, Fotos P, Goll KT. Retrospective assessment of osteomyelitis: etiology, demographics, risk factors and management in 35 cases. Oral Surg Oral Pathol 1992;74:149–154 11. Marx RE. Chronic osteomyelitis of the jaws. Oral Maxillofac Surg Clin North Am 1991;3:367–369 12. Lorè B, Gargari M, Ventucci E, et al. A complication following tooth extraction: chronic suppurative osteomyelitis. Oral Implantol 2013;6:43–47 13. Trampuz A, Zimmerli W. Diagnosis and treatment of infections associated with fracture-fixation devices. Injury 2006;37:S59–S66 14. Wright JA, Nair SP. Interaction of staphylococci with bone. Int J Med Microbiol 2010;300:193–204 15. Wida A, Claro T, Foster TJ, et al. Staphylococcus aureus protein A plays a critical role in mediating bone destruction and bone loss in osteomyelitis. PLoS One 2012;7:e40586 16. Sanchez CJ Jr, Ward CL, Romano DR, et al. Staphylococcus aureus biofilms decrease osteoblast viability, inhibits osteogenic differentiation, and increases bone resorption in vitro. BMC Musculoskelet Disord 2013;14:187 17. Clauss M, Trampuz A, Borens O, et al. Biofilm formation on bone grafts and bone graft substitutes: comparison of different materials by a standard in vitro test and microcalorimetry. Acta Biomater 2010;6:3791–3797 18. Misch CM. Autogenous bone: is it still the gold standard? Implant Dent 2010;19:361 19. Zins JE, Langevin CJ, Nasir S. Controversies in skull reconstruction. J Craniofac Surg 2010;21:1755–1760 20. Van Blitterswijk CA, Grote JJ, De Groot K. The biological performance of calcium phosphate ceramics in an infected implantation site: I. Biological performance of hydroxyapatite during Staphylococcus aureus infection. J Biomed Mater Res 1986;20:989 21. Nickel JC, Ruseska I, Wright JB, et al. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Therapeutic 1985;27:619–624 22. Sanchez CJ Jr, Mende K, Beckius ML, et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 2013;29:13–47 23. Patel R. Biofilms and antimicrobial resistance. Clin Orthop Rel Res 2005;437:41–47 24. Koorbusch GF, Deatherage JR, Curé JK. How can we diagnose and treat osteomyelitis of the jaws as early as possible? Oral Maxillofac Surg Clin North Am 2011;23:557–567 25. Mayberry-Carson KJ, Tober-Meyer B, Smith JK, et al. Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus. Infection and Immunity 1984;43:825–833 26. O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000;54:49–79 27. Jenkinson HF, Lappin-Scott HM. Biofilms adhere to stay. Trends Microbiol 2001;9:9–10 28. Rickard AH, Gilbert P, High NJ, et al. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 2003;11:94–100 29. Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop Relat Res 2005;437:7–11
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
Autogenous Bone Grafts Contamination After Exposure to the Oral Cavity Hugo Nary Filho, PhD,* Tábata Fernandes Pinto,† Caio Peixoto de Freitas,* Paulo Domingos Ribeiro-Junior, PhD,* Pâmela Letícia dos Santos, PhD,* and Mariza Akemi Matsumoto, PhD* Abstract: The purpose of this paper was to analyze specimens of autogenous bone block grafts exposed to the oral cavity after ridge reconstructions. Specimens of chronic suppurative osteomyelitis (CSO) of the jaws were used as comparison for bacterial colonization pattern. For this, 5 specimens of infected autogenous bone grafts were used and 10 specimens of CSO embedded in paraffin were stained with Brown and Brenn technique and analyzed under light microscopy. The results showed a similar colonization pattern in both situations, with the establishment of bacterial biofilm and the predominance of Gram-positive bacteria. The conclusion was that the similarity in bacterial distribution and colonization between autogenous bone grafts and CSO stresses the necessity of more invasive procedures for the treatment of the autogenous bone grafts early exposed to the oral cavity. Key Words: Bone reconstruction, autogenous bone graft, bacterial biofilm, osteomyelitis (J Craniofac Surg 2014;25: 412–414)
T
ooth loss is followed by important changes and remodeling of alveolar ridge, eventually making the rehabilitation with endosseous implants extremely difficult due to the remaining width and height bone volume.1 In face of these situations, literature provide a number of options for the reconstruction of atrophic ridges, among them the use of autogenous, homogenous, and heterogeneous bone grafts, along with the alloplastic implants.2 Autogenous bone graft is considered the first option due to its favorable properties, extensively described elsewhere3 resulting in better postoperative conditions and avoiding immunological
What Is This Box? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code links to the online version of the article.
From the *Department of Oral Biology Post Graduation, and †Dentistry Course, University do Sagrado Coração (USC), Bauru, São Paulo, Brazil. Received December 1, 2013. Accepted for publication December 28, 2013. Address correspondence and reprint requests to Mariza Akemi Matsumoto, PhD, Departament of Pró-Reitoria de Pesquisa e Pós-graduação, Universidade Sagrado Coração, Rua Irmã Arminda, 10-50, 17011-160 Bauru, SP, Brazil; E-mail: [email protected] The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000000682
412
incompatibilities.4,5 However, this kind of graft presents some limitations such as donor-site morbidity, increased surgical time, and limited available bone.6 Complications at the recipient area also occur, mainly related to contamination of the graft due to its early exposure usually resulting in failure of the procedure.7 Although it represents a complication that most of the reconstructive oral surgeons have already, or will, faced in their clinical practice, only a few reports are cited in literature.8,9 One of the most important infectious diseases of the bones, including the jaws, is osteomyelitis caused by the installation of bacterial biofilm in the medullary space that can spread to the periosteum, cortical bone, and soft tissues.10 Its classification in acute or chronic suppurative osteomyelitis (CSO) is dependent upon the duration of the disease.11 Sequestrectomy of the necrotic tissue and debridement of the surrounding bone and systemic antibiotic therapy is the treatment of choice, sometimes associated to hyperbaric oxygen therapy.12 Staphylococci are considered the most infecting microorganisms of bone tissue13–15 being the species aureus the most commonly found. In an in vitro study, Sanchez et al (2013)16 observed the behavior of osteoblastic cells in Staphylococcus aureus biofilm conditioned media and revealed a reduced osteoblast differentiation and viability, along with an increase in apoptosis with an up-regulated expression of the receptor activator of nuclear factor kappa-B ligand, responsible for recruitment and activation of the osteoclasts. In an interesting study, Clauss et al (2010)17 compared early and mature S. aureus biofilm formation on the surface of fresh and fresh-frozen human bone grafts from femoral heads, and processed human and bovine bone grafts, finding a decreased biofilm density on fresh and fresh-frozen grafts after 24 hours. Although minimal structural architectural differences were found among the materials, biological characteristics seemed to be relevant, as the maintenance of serum proteins and the presence of bone marrow content on fresh grafts’ surface, which are lost in the processed bones. In this way, similarities regarding the microorganism and evolution of bone infection caused by the installation of the biofilms are evident. In this way, the present study aimed to analyze the histological pattern of mature biofilm in early exposed bone grafts and to compare them with CSO, in an attempt to guide clinicians to a more appropriate resolution.
MATERIALS AND METHODS Samples from 5 patients who underwent horizontal alveolar reconstruction (onlay) with autogenous bone grafts retrieved from the mandibular ramus (Table 1) were obtained. All the patients presented early exposure of the block grafts due to suture dehiscence, up to 1 month after the reconstructive procedure, which were immediately removed and prepared for a further reconstruction procedure. The removed blocks were fixed in 10% buffered formalin and decalcified in 4% EDTA, to be processed under histologic routine technique, sectioned in their longer axis and stained with Brown and Brenn to
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Autogenous Bone Grafts Contamination
TABLE 1. Characterization of the Patients Submitted to Autogenous Bone Grafts Alveolar Ridge Reconstruction Patient
Gender
Age
Donor Site
Receptor Site
1
Male Male Male Male Female
Non-informed 44 63 68 71
Mandibular symphysis Iliac crest Mandibular body and angle Iliac crest Iliac crest
Mandible Mandible Mandible Mandible Mandible
2 3 4 5
evidence Gram-positive and Gram-negative bacteria. The slices were analyzed under light microscopy for morphological characterization of the grafts. In the same way, and for comparative purposes, CSO paraffin-embedded specimens were selected from the archives of Oral Pathology Laboratory from the Sagrado Coração University (Bauru, SP, Brazil) that also could be clinically characterized. These specimens were re-sectioned and stained by the same technique of the bone grafts, used as a parameter for the microscopic analysis.
RESULTS Autogenous Bone Block Grafts In the specimens of autogenous bone grafts fragments (Fig. 1), nonviable bone were present, with no signs of bone formation or remodeling. Bone surfaces were irregular, probably due to previous osteoclastic activity. Organized bacterial biofilms attached on bone surface were constituted predominantly of Gram-positive bacteria, stained in purple. However, eventual osteocytes lacunas were filled by Gram-negative bacteria, stained in red (Fig. 2A–C).
CSO CSO specimens revealed nonviable bone tissue, characterized by the absence of osteoblasts, lining cells, and osteocytes in bone matrix. No evidence of remodeling or bone formation was noted. Bone surface was irregular and covered by bacterial biofilms with the predominance of Gram-positive bacteria, stained in purple. Biofilms could be visualized filling bone lacunae and Havers channels. Intense mononuclear and neutrophilic infiltrate was observed in medullar spaces (Fig. 3A–C).
FIGURE 1. Autogenous onlay bone graft retrieved after contamination and exposure.
FIGURE 2. Autogenous bone grafts—A, nonviable bone fragments (B) showing irregular surface covered by Gram-positive bacterial biofilm (arrows); B, well-established Gram-positive biofilm covering bone surfaces (arrows); C, Gram-negative biofilms could be seen filling some bone lacunas (small arrows) (Brown and Brenn; bars = 100 μm).
DISCUSSION Autogenous bone grafts are still considered the gold standard for functional and aesthetic reconstructions of atrophic alveolar ridges in implantology18,19; however, this procedure can lead to transoperative and postoperative complications, the last one being more frequent and associated to graft failure. Some of them are reported in literature, as presented by Schwartz-Arad and Levin (2005)8 in an analysis involving 10 patients who underwent extensive maxillary reconstructions using intraoral block bone grafts resulting in 2 cases of minimal graft exposure and one partially failed, being partially removed. In another report, 64 onlay bone grafts were analyzed, with 12.5% of them considered as failure due to their exposure or removal.9 Unfortunately, a lack of details about these complications such as the time of the grafts exposure or removal, or the first therapeutic actions, make difficult to delineate a preventive or treatment protocol. The contamination and infection of exposed autogenous bone grafts in the oral cavity are understandable when one considers autogenous bone grafts as temporary foreign bodies since they are free of vascularization and present a reduced resistance against bacterial infection, as stated by Van Blitterswijk et al (1986).20 In the present study, the pattern of bacterial colonization in autogenous bone exposed to the oral cavity due to suture dehiscence was compared to
FIGURE 3. Chronic suppurative osteomyelitis—A, bone fragments showing no vitality, with absence of bone cells (B); B, bone surface covered by established biofilm predominantly constituted by Gram-positive bacteria stained in purple (arrows); C, note intense neutrophilic infiltrate in medullar spaces (*) (Brown and Brenn; bars = 100 μm).
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
413
The Journal of Craniofacial Surgery • Volume 25, Number 2, March 2014
Filho et al
CSO. The pattern of biofilm installation can play an important role in the treatment of infectious conditions that affect bone tissue. Systemic antibiotic therapy, an even topic, can control the symptoms of the infection, but is limited in eliminating the bacteria that are attached in the biofilm. Besides, some studies have been shown that the decrease in nutrients and oxygen is a condition that transmutate some bacteria to a state of resistant phenotype, and to constitute a biofilm with genes resistant to antimicrobial drugs.21,22 For these reasons, this kind of infection frequently reappears after antibiotic therapy and is more efficiently resolved with the mechanical removal of the affected tissue.13,23,24 Although infected bone grafts and CSO constitute different pathological conditions, it is clear that bone tissue commitment is quite similar, as shown by the microscopic pattern of biofilm distribution and quality in both conditions as evidenced in this study. The predominance of Gram-positive bacteria agrees with the prevalence of the genus Staphylococci in both conditions. The presence of the biofilm in bone surface and lacunae, the mineralized matrix, and the glycocalix formation25–29 makes easy the understanding of the poor action of drugs and the necessity of surgical removal of the affected bone. The conclusion was that the similarity in bacterial distribution and colonization between exposed bone block grafts and CSO stresses the necessity of more invasive procedures for their resolution. The total removal of the compromised bone seems to be the more indicated attitude, considering the difficulty in reverting such an organized contamination in a poor vascularized tissue. ACKNOWLEDGMENTS The authors are thankful to Maira Cristina Rondina Couto for her histotechnical assistance. This work was supported by grants from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).
REFERENCES 1. Sbordone L, Toti P, Fabris GM, et al. Implant Sucess in sinus lifted maxillae and native bone: a 3-year clinical and computerized tomographic follow-up. Int J Oral Maxillofac Implants 2009;24:316–324 2. Esposito M, Grusovin MG, Felice P, et al. The efficacy of horizontal and vertical bone augmentation procedures for dental implants—a Cochrane systematic review. Eur J Oral Implantol 2009;2:167–184 3. Zouhary KJ. Bone graft harvesting from distant sites: concepts and techniques. Oral Maxillofac Surg Clin North Am 2010;22:301–316 4. Keller E, Tolman DE, Eckert S. Surgical implants for bone reconstruction of advanced maxillary commitment autogenous onlay block bone grafts and osseointegrated endosseous implants: a 12-year study of 32 consecutive patients. Int J Oral Implantes Maxillofac 1997;14:197–209 5. Cordaro L, Amade DS, Cordaro M. Clinical results of alveolar ridge augmentation with mandibular block bone grafts in partially edentulous patients prior to implant placement. Clin Oral Implants Res 2002;13:103–111 6. McAllister DR, Joyce MJ, Mann BJ, et al. Allograft update: the current status of tissue regulation, procurement, processing and sterilization. Am J Sports Med 2007;35:2148–2158 7. Bahat O, Fontanesi RV. Complications of graft in atrophic jaws edentulous or partially edentulous. Int J Periodontics Restorative Dent 2001;21:487–495
414
8. Schwartz-Arad D, Levin L. Intraoral autogenous block onlay bone grafting for extensive reconstruction of atrophic maxillary alveolar ridges. J Periodontol 2005;76:636–641 9. Schwartz-Arad D, Levin L, Sigal L. Surgical success of intraoral autogenous block onlay bone grafting for alveolar ridge augmentation. Implant Dent 2005;14:131–138 10. Koorbusch GF, Fotos P, Goll KT. Retrospective assessment of osteomyelitis: etiology, demographics, risk factors and management in 35 cases. Oral Surg Oral Pathol 1992;74:149–154 11. Marx RE. Chronic osteomyelitis of the jaws. Oral Maxillofac Surg Clin North Am 1991;3:367–369 12. Lorè B, Gargari M, Ventucci E, et al. A complication following tooth extraction: chronic suppurative osteomyelitis. Oral Implantol 2013;6:43–47 13. Trampuz A, Zimmerli W. Diagnosis and treatment of infections associated with fracture-fixation devices. Injury 2006;37:S59–S66 14. Wright JA, Nair SP. Interaction of staphylococci with bone. Int J Med Microbiol 2010;300:193–204 15. Wida A, Claro T, Foster TJ, et al. Staphylococcus aureus protein A plays a critical role in mediating bone destruction and bone loss in osteomyelitis. PLoS One 2012;7:e40586 16. Sanchez CJ Jr, Ward CL, Romano DR, et al. Staphylococcus aureus biofilms decrease osteoblast viability, inhibits osteogenic differentiation, and increases bone resorption in vitro. BMC Musculoskelet Disord 2013;14:187 17. Clauss M, Trampuz A, Borens O, et al. Biofilm formation on bone grafts and bone graft substitutes: comparison of different materials by a standard in vitro test and microcalorimetry. Acta Biomater 2010;6:3791–3797 18. Misch CM. Autogenous bone: is it still the gold standard? Implant Dent 2010;19:361 19. Zins JE, Langevin CJ, Nasir S. Controversies in skull reconstruction. J Craniofac Surg 2010;21:1755–1760 20. Van Blitterswijk CA, Grote JJ, De Groot K. The biological performance of calcium phosphate ceramics in an infected implantation site: I. Biological performance of hydroxyapatite during Staphylococcus aureus infection. J Biomed Mater Res 1986;20:989 21. Nickel JC, Ruseska I, Wright JB, et al. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Therapeutic 1985;27:619–624 22. Sanchez CJ Jr, Mende K, Beckius ML, et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 2013;29:13–47 23. Patel R. Biofilms and antimicrobial resistance. Clin Orthop Rel Res 2005;437:41–47 24. Koorbusch GF, Deatherage JR, Curé JK. How can we diagnose and treat osteomyelitis of the jaws as early as possible? Oral Maxillofac Surg Clin North Am 2011;23:557–567 25. Mayberry-Carson KJ, Tober-Meyer B, Smith JK, et al. Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus. Infection and Immunity 1984;43:825–833 26. O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol 2000;54:49–79 27. Jenkinson HF, Lappin-Scott HM. Biofilms adhere to stay. Trends Microbiol 2001;9:9–10 28. Rickard AH, Gilbert P, High NJ, et al. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 2003;11:94–100 29. Costerton JW. Biofilm theory can guide the treatment of device-related orthopaedic infections. Clin Orthop Relat Res 2005;437:7–11
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
