Periodontology 2000, Vol. 67, 2015, 7–12 Printed in Singapore. All rights reserved
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PERIODONTOLOGY 2000
A Latin American perspective of periodontology G. C A F F E S S E R A UL
The pioneers ‘After having dedicated eleven years practicing different surgical methods for the treatment of paradentosis, we have been able to compare de visu, in many cases, the clinical and radiographic aspects of pyorrheic lesions with their macroscopic anatomical changes, since the flap surgical approach permits assessing the characteristics of the bony lesion and those of the affected area’. This statement was written by Fermin A. Carranza Sr. as the introduction to his Doctoral Thesis ‘Surgical Treatment of Paradentosis (Alveolar Phyorrea)’ approved at the Medical School, National University of Buenos Aires, Argentina, and published in 1935 (7). The truth is that Latin American dentists have been pioneers in the field of periodontology. Although their early communications were devoted to the nonsurgical treatment of periodontitis, it was Carranza Sr. who pioneered the development of the knowledge of periodontics in Argentina and Latin America. Following Neumann’s publications, Carranza Sr. began treating periodontal disease using the flap approach and, in 1928, published his first article related to the surgical treatment of ‘alveolar pyorrhea’ (6). In 1942, a few years after completing his doctoral thesis, he published his classical article ‘When and why bone should be sacrificed in the treatment of Paradentosis’ (5). In this article he presented drawings and cases for which he recommended removal of alveolar bone. Those indications were very similar, and in certain cases identical, to those published by Schluger in his classical publication of 1949 (22). The language barrier and the geographical distance contributed to the lack of communication between those two researchers. Aside from his interest in the clinical area, and being a devoted clinician, Carranza Sr. worked closely with his thesis mentor, Rodolfo Erausquin, who was
an eminent oral pathologist. Together they studied autopsy specimens to describe the histopathology of periodontal diseases (2, 3, 8, 10). These studies constituted the basis for their understanding of the periodontal disease process and for Carranza’s future approach to treatment and his emphasis on ‘reattachment’ in publications many years later. Carranza’s influence transcended the early developments of the periodontal discipline and the boundaries of Latin America. He lectured extensively in Argentina and in other Latin American countries, as well as in Europe and the USA. Carranza Sr. formed a large group of followers, who became leaders in the field of periodontics. The strong development of periodontics in Argentina was not an isolated event. At the same time, across the Andes, in Chile, another group was promoting the development of periodontics. In 1924, at the School of Biological and Medical Sciences at the University of Chile in Santiago, a ‘Department of Parodontics’ was established. This was probably one of the first, if not the first, department in the world solely devoted to periodontal teaching. Alfonso Leng was in charge, and in 1932 was appointed Full Professor of Parodontics. Juan Villavicencio Rubio joined him in 1926. When the School of Dentistry was established, both continued to be responsible for the teaching of periodontics at all different levels and carried on research until their retirement from academia. Simultaneously, in Uruguay, a neighboring state of Argentina, other individuals were also devoting their professional career to periodontics, of whom Francisco M. Pucci and Jorge Mazzoni were the leaders (17, 18, 20). In 1940, Francisco M. Pucci published ‘Paradencio – Patologia y Tratamiento’, a comprehensive treatise with several editions, almost 700 pages long and wholly dedicated to periodontics, which for many years was the leading such text in Latin America (19).
7
Caffesse
The interest devoted to periodontics in the southern part of Latin America spread, over time, to other countries in the region. Pedro Ayllon (Peru), Focion Febres Cordero and Raul Vincentelli (Venezuela), Guillermo Gamboa, Rafael Lozano and Antonio Ruiz (Mexico), Cesio de Padua Lima and Rugerpe A. Pedre~ o, Jose Rezk and ira (Brazil) and Guillermo London Carlos de Castro (Colombia), among many others, represented the nuclei of individuals in their own countries who were educating the dental profession on the importance of periodontics for oral and systemic health. However, it is undisputable that the trio of Fermin A. Carranza Sr., Alfonso Leng and Francisco M. Pucci constitute the historic core who greatly influenced all Latin America and beyond, and that these individuals were responsible for the high level of development and consideration that periodontics has gained within dentistry in that part of the world.
Current periodontics The scope of current periodontics in Latin America is, of course, quite different from that of the early decades of the last century. Education, research and clinical practice have evolved, a formal postgraduate program in periodontics has been established in many universities of Latin America and many individuals have traveled to US and European universities to complete their formal training, including research. Fortunately, many have returned to their home countries and have continued their academic and investigative activities with some financial support from governments. Consequently, the volume of presentday research in periodontics from Latin America is significant and thus selecting the topics and contributors for this volume of Periodontology 2000 was difficult. The papers included here represent only a small sample of the myriad of periodontal research that is taking place throughout Latin America. The prevalence and the severity of periodontal diseases in Latin America have been topics of research for many years; however, even today we do not have a clear understanding of the magnitude of these diseases throughout the continent. Oppermann et al. (15) report on the epidemiology of adult periodontal diseases, and Botero et al. (4) report on the epidemiology of periodontal diseases in children and adolescents. Both articles point out the heterogeneity of the studies performed, most of which are cross-sectional, with methodologies and periodontal assessment indices that are difficult to compare. In spite of the
8
difficulties, it is clear that the prevalence of periodontal disease is very high in Latin America and it relates to all the known risk factors for the disease. Some demographic factors assume particularly great importance for periodontal disease in Latin America. There exist marked variations in race and ethnicity within and among the countries, and there are significant disparities among the populations in terms of education and socio-economic status, with more than half of the population living below the poverty line with minimal access to dental care. In general, the percentage of periodontally healthy subjects decreases with age, along with an increase in plaque and calculus accumulation. Periodontitis increases with age and is more prevalent in male subjects, heavy smokers and individuals of low socio-economic status. A 5-year longitudinal epidemiological study from Brazil estimated an average loss of attachment of 0.33 mm/ year at the worst interdental site of each tooth and of 0.10 mm/year at the remaining four interdental sites per tooth. These values fall midway between those reported for populations with minimal dental care and those reported for well-maintained populations. Botero et al. (4) have reviewed periodontal diseases in children and adolescents and found a scarcity of periodontal studies of young people in Latin America. Gingivitis is prevalent in children and adolescents, but other manifestations of periodontal disease can also be found, including aggressive periodontitis, acute necrotizing ulcerative gingivitis and herpesvirus and fungal infections. The overall mean prevalence of gingivitis in Latin America is reported to be 34.7%, varying among individual countries from 24 to 77%. The prevalence of bleeding on probing is reported to be 15–35%. Aggressive periodontitis in adolescents is approximately 2% and incipient periodontitis is 20%. Acute necrotizing ulcerative gingivitis and necrotizing ulcerative periodontitis, leading to noma/cancrum oris, have been documented in children in Colombia, who had predisposing factors such as acute herpetic gingivostomatitis or measles, combined with malnutrition and poor oral hygiene. The high prevalence of gingivitis and its possible progression to periodontitis stresses the importance of early diagnosis and treatment, and the need for public campaigns to educate the population about the benefits of controlling gingivitis at an early age. The inter-relationship between biofilm microorganisms and the host response has attracted a significant amount of research globally, including Latin America. Contreras et al. (9) present an updated review of studies from Latin America on infectious agents in periodontal disease. Owing to the great
Latin American perspective of periodontology
ethnic diversity and challenging economy, people in Latin America may have an elevated risk of acquiring periodontal pathogens and developing periodontal disease. Black people and Mestizos are frequently colonized with Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. The ‘red complex’ bacteria and A. actinomycetemcomitans are closely associated with chronic and aggressive periodontitis, but may show an unequal distribution in different Latin American populations and countries. Other putative periodontal pathogens include gram-negative enteric rods and herpesviruses. Herpes simplex virus type 1, human cytomegalovirus, Epstein–Barr virus and other herpesviruses can be detected in gingival crevicular fluid and within inflamed gingiva, as well as in other areas of the mouth, and have been linked to chronic and aggressive periodontitis and to acute necrotizing ulcerative gingivitis. Hopefully, increased insights into the periodontal microbiota may lead to more affordable periodontal treatments to counteract the almost ‘epidemic’ nature of destructive periodontal disease in low-income individuals of Latin America. The relationship between periodontal diseases and systemic conditions has been a topic of research onand-off for the past century. Systemic conditions can affect the prevalence and progression of periodontitis, but, at the same time, periodontitis may be a significant risk factor for several systemic conditions, including cardiovascular diseases, stroke, low birth weight and preterm birth, diabetes, osteoporosis, chronic obstructive pulmonary disease and pneumo pez et al. (12) address the effects of periodonnia. Lo tal disease on preterm birth rate. Although several papers have been written on this association, and intervention studies have been performed, the reported results are controversial and published systematic reviews and meta-analyses have not helped to clarify the issue. The methodological aspects of the individual randomized clinical trials included in the meta-analyses, may not have clearly determined and controlled inclusion and exclusion criteria, periodontal disease status, confounding factors for preterm birth, the periodontal effectiveness of intervention regimes, and specific end-points as thera pez et al. (12) have evaluated peutic outcomes. Lo the conclusion of six meta-analyses, four of which found no effect and two of which did find an effect of periodontal treatment on preterm birth rate. pez et al. (12) suggest that trials with a proper defLo inition of periodontitis, including probing pocket depth and clinical attachment level, and effective control of periodontal infections have indeed
demonstrated a reduced rate of preterm birth following periodontal therapy. The use of systemic antibiotics in periodontal treatment has been a topic of controversy. Feres et al. (11) present a comprehensive review, emphasizing their own clinical and microbiological research, including randomized clinical trials of 1–2 years’ duration. They stress the ecological concept that the entire mouth ought to be regarded as a unit of bacteria living in biofilm accumulations. That notion supports the use of systemic, rather than local, antibiotic therapy for the control of pathogenic bacteria residing in different sites of the oral cavity. One of the main concerns with the use of systemic antibiotics has been the development of bacterial resistance; however, according to their research, resistance is only transient, and by 3 months bacterial-sensitivity patterns return to baseline values. The authors stress the importance of combating the ‘red complex’ pathogens and A. actinomycetemcomitans, as well as other newly recognized microbial species, in periodontal disease. Based on randomized clinical trials designed to evaluate the clinical and microbiological effects of various systemic antibiotics, Feres et al. (11) conclude that young individuals with aggressive periodontitis and adults with generalized chronic periodontitis can benefit from a 14-day treatment with amoxicillin plus metronidazole combined with local mechanical therapy. However, that treatment seems to be less effective in smokers because of an inadequate response of the ‘orange complex’ bacteria, which serve as precursors for the colonization of the major pathogenic bacteria of the ‘red complex’. A failure of periodontal therapy to suppress the periodontopathic microbiota markedly may provide an additional explanation for the reduced treatment response in smokers. Feres et al. (11) utilize their reported data to support and promote the use of systemic antibiotics during the active phase of periodontal therapy. Smoking comprises a very significant risk factor for the overall health of an individual, although it is one of the lifestyles that can be modified. The prevalence of smoking in Latin America is not well established, but is estimated to be in the magnitude of 8–10%, and is particularly widespread in populations of low socio-economic and educational standing. Female subjects in Latin America seem to smoke more than female subjects in the rest of the world, and the habit begins in adolescence. Another significant problem is passive smoking, both at home and at work – national campaigns promoting smoke-free places have had only limited success and airborne nicotine contamination has been demonstrated in some of the
9
Caffesse
important metropolis centers. Nociti et al. (14) present a thorough review on the effect of smoking on periodontal disease, supported by their own in-vitro and in-vivo studies and by other published research. Clinical, microbiological and immunological data are discussed to explain the increased propensity of smokers to experience destructive periodontal disease. Clinically, smokers exhibit more severe loss of alveolar bone, periodontal attachment loss, gingival recession and tooth loss. The number of cigarettes and years of smoking seem to correlate with the progression of periodontitis. Microbiologically, the ‘red complex’ of pathogens and A. actinomycetemcomitans have been identified both in smokers and in nonsmokers; whether the level of these bacteria is different in smokers than in nonsmokers has still to be established. The same pathogens may trigger the production of lower amounts of proinflammatory cytokines, and subsequently relatively little gingivitis, in smokers. The immunological mechanisms of periodontal breakdown in smokers are not clear. Tobacco is cytotoxic, containing potent toxins such as nicotine, carbon monoxide and reactive oxidants that can affect both innate and adaptive immune systems. Therapeutically, smokers show an unfavorable response to nonsurgical and surgical therapy, and to periodontalregenerative and plastic procedures; however, the negative effects of smoking seem to be reversible, with former smokers responding to therapy better than current smokers. Obviously, smoking cessation should constitute a standard part of periodontal therapy. Periodontal regeneration is an important area of research, and significant progress has been made in understanding the cellular and molecular events of regeneration. Periodontal healing and regeneration depends on the availability of proper cells, extracellular matrix or scaffold, and growth and differentiation factors. Research on periodontal regeneration in Latin America has involved cementoblasts, growth factors and mesenchymal stem cells. The article by Arzate et al. (1) evaluates the role of cementum molecules in the formation, repair and regeneration of the periodontium. The authors review collagen and noncollagen proteins of cementum, and describe in detail the cementum protein type 1, which is responsible for 70% of the mitogenic activity in cementum. Cementum protein type 1 is expressed in human gingival fibroblasts and periodontal ligament cells, is released during demineralization and repair, and seems to regulate the growth and composition of apatite crystals. The enamel-associated proteins amelogenin and enamelin are also found in cementum and may be involved in acellular cementum formation.
10
Smith et al. (23) address the topic of growth factors and cytokines and their ability to bind to cell receptors, activate transmembrane signaling and trigger the orderly sequence of intracellular responses involved in periodontal healing. Smith et al. (23) discuss growth factors associated with periodontal healing and regeneration, including transforming growth factor-beta, platelet-derived growth factor and bone morphogenetic proteins. Transforming growth factorbeta supports extracellular matrix deposition and remodeling during wound healing. Platelet-derived growth factor stimulates cell proliferation and chemotaxis, and is believed to be involved in the initial stages of healing. Bone morphogenetic proteins belong to the transforming growth factor-beta superfamily and participate in cartilage and bone formation, remodeling and repair. Sanz et al. (21) discuss the use of mesenchymal stem cells from the oral cavity in tissue regeneration. Oral stem cells are present in the pulp tissue of permanent teeth. The pulpal stem cells can differentiate into odontoblasts, osteoblasts, chondrocytes, adipocytes, neurocytes and pluripotent stem cells, and have the potential to develop dentin/pulp complexes. Stem cells isolated from the apical papilla of developing teeth can differentiate into chondrogenic, osteogenic or adipogenic lineages, display dentinogenic markers and induce root formation. Stem cells from the periodontal ligament can differentiate into cementoblasts. Finally, stem cells are present in gingival connective tissue. Gingivalderived stem cells are readily harvested and can differentiate into osteogenic, chondrogenic and adipogenic lineages. The approaches to tissue regeneration presented above may one day lead to the development of effective and reproducible regenerative therapies in periodontics. Lasers have been used in periodontics since their introduction in the medical field. When used in surgery, lasers may increase blood flow and promote cell proliferation and healing by recruiting cytokines and growth factors to the wound. Passanezi et al. (16) review current concepts and uses of high- and lowintensity lasers in periodontal therapy, mainly based on findings reported by Latin American researchers. High-intensity lasers have been used in nonsurgical periodontal therapy for root biomodification and in the treatment of root hypersensitivity, and low-intensity lasers have been used to improve regenerative procedures and in antimicrobial photodynamic therapy. However, the use of laser treatment in periodontics is surrounded by controversy regarding the real clinical benefits, as the research results are conflicting and difficult to extrapolate to clinical practice. Con-
Latin American perspective of periodontology
tributing to the confusion is research reports of laser units with different wavelength and irradiation settings, which are important determinants of the clinical outcome. Nonetheless, laser treatment seems to have great patient acceptance and may be applied to individuals who object to or are recalcitrant to traditional periodontal therapy, as in diabetic, immunocompromised or disabled patients. Basic and clinical research in areas that may be peripheral, but still have significance and interest for periodontics, is also underway in Latin America. Monti-Hughes et al. (13) report on research being conducted on ‘field cancerization’ using the hamster cheek pouch model. Field cancerization refers to the changes that carcinogens, such as tobacco and alcohol, can induce in the oral mucosa, producing molecular changes that can be detected by histochemical techniques in biopsies, before histological modifications can be identified. Carcinogens applied in solution on the mucosal surface of the hamster cheek pouch induce alterations mimicking those detected in the human oral mucosa. The hamster model has also been proposed and validated for testing Boron Neutron Capture Therapy, a novel approach in the treatment of oral cancer, and clinical trials are already underway for certain tumor types and localizations. Boron Neutron Capture Therapy has been proposed as a more selective and effective approach in the treatment of head and neck cancer. The therapy administers boron carriers, which are taken up primarily by neoplastic cells, followed by irradiation with a neutron beam. The hamster cheek pouch model was also adapted for long-term studies of field cancerization, and the authors were able to show the inhibitory effect of Boron Neutron Capture Therapy on the development of tumors in field cancerized tissues, with acceptable levels of slight mucositis as a dose-limiting side-effect. In conclusion, this volume of Periodontology 2000 reviews the epidemiology, the etiopathology and the treatment of periodontal diseases in Latin America. Emphasis is placed on the microbiology of periodontitis, the effect of smoking and the benefits of systemic antibiotics and laser treatment. In addition, basic research in new areas of regeneration and in cancer therapy is also presented. The present volume of Periodontology 2000 is a vivid representation of the variety and the high quality of research that is carried out in laboratories, institutes and universities throughout Latin America. Latin America faces the same periodontal-disease concerns as in other parts of the world, but also has to confront unique challenges in a large
population of socio-economically disadvantaged individuals who receive little or no periodontal healthcare. The articles presented here will hopefully stimulate further studies on periodontal disease prevention and treatment to help combat the high level of edentulism in Latin America.
Acknowledgments Appreciation is expressed to the following colleagues and friends who helped with historical information: Drs Fermın A. Carranza Jr., Mauricio Echeverri, Ernesto Muller, Antonio W. Sallum, Juan J. Villavicencio n. R and Agustın Zero
References 1. Arzate H, Zeichner-David M, Mercado-Celis G. Cementum proteins: role in cementogenesis, biomineralization, periodontium formation and regeneration. Periodontol 2000 2015: 67: 211–233. 2. Ballbe R, Carranza FA, Erausquin R. Los paradencios del caso numero 7. Rev Odont 1941: 29: 600–635. 3. Ballbe R, Carranza FA, Erausquin R. Los paradencios del caso numero 8. Rev Odont 1942: 30: 606–642. € sing C, Duque A, Jaramillo A, 4. Botero JE, Kuchenbecker Ro Contreras A. Periodontal disease of children and adolescents in Latin America. Periodontol 2000 2015: 67: 34–57. ndo y por que sacrificar hueso en el tra5. Carranza FA. Cua tamiento de la paradentosis? Rev Odont 1942: 30: 646–653. 6. Carranza FA. La cirugıa en el tratamiento de la piorrea alveolar. Tribuna Odontologica 1928: 12: 21–34. rgico de la paradentosis 7. Carranza FA. Tratamiento quiru (Piorrea alveolar). Tesis de Doctorado. Universidad Naciondicas, 1935. al de Buenos Aires, Facultad de Ciencias Me 8. Carranza FA, Erausquin R. Paradencio normal. Rev Odont (Buenos Aires) 1938: 26: 433–457. 9. Contreras A, Moreno SM, Jaramillo A, Pelaez M, Duque A, Botero JE, Slots J. Periodontal microbiology in Latin America. Periodontol 2000 2015: 67: 58–86. 10. Erausquin R, Carranza FA. Primeros hallazgos paradentosicos. Rev Odont 1939: 29: 486–498. 11. Feres M, Faveri M, Figueredo LC, Soares GMS. Systemic antibiotics in the treatment of periodontitis. Periodontol 2000 2015: 67: 131–186. pez NJ, Uribe S, Martinez B. Effect of periodontal treat12. Lo ment on preterm birth rate: a systematic review of meta-analyses. Periodontol 2000 2015: 67: 87–130. 13. Monti-Hughes A, Aromando R, Perez MA, Schwint AE, Itoiz ME. The hamster cheek pouch model for field cancerization studies. Periodontol 2000 2015: 67: 292–311. 14. Nociti FH Jr, Casati MZ, Duarte PM. Current perspective of the impact of smoking on the progression and treatment of periodontitis. Periodontol 2000 2015: 67: 187–210. € sing CK, Susin C. Epidemiol15. Oppermann RV, Haas AN, Ro ogy of periodontal diseases in adults from Latin America. Periodontol 2000 2015: 67: 13–33.
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Caffesse 16. Passanezi E, Damante CA, Rubo de Rezende ML, Greghi SLA. Lasers in periodontal therapy. Periodontol 2000 2015: 67: 268–291. l es el tratamiento ma s racional de la para17. Pucci FM. Cua dentosis? Rev Odont 1936: 24: 15–28 (March-May). n y reaccio n del cemento y de la membra18. Pucci FM. Funcio na peridentaria. Rev Odont 1934: 22: 119–130. 19. Pucci FM. Paradencio – Patologıa y Tratamiento. In: Garcia dica, Morales J, editor. Editorial. Montevideo, Uruguay, Me 1940: 697 pages. 20. Pucci FM. Paradenciopatias: Gingivitis y preparadentitis: paradentitis marginales y paradentosis malignas. Rev Odont 1940: 28: 913–934.
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n FS, Chaparro AP. Mesenchymal stem cells 21. Sanz AR, Carrio from the oral cavity and their potential value in tissue engineering. Periodontol 2000 2015: 67: 251–267. 22. Schluger S. Osseous resection – A basic principle in periodontal surgery. Oral Surg Oral Med Oral Pathol 1949: 2: 316–325. ceres M, Martınez J. Research in 23. Smith PC, Martınez C, Ca growth factors in periodontology. Periodontol 2000 2015: 67: 234–250.
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PERIODONTOLOGY 2000
A Latin American perspective of periodontology G. C A F F E S S E R A UL
The pioneers ‘After having dedicated eleven years practicing different surgical methods for the treatment of paradentosis, we have been able to compare de visu, in many cases, the clinical and radiographic aspects of pyorrheic lesions with their macroscopic anatomical changes, since the flap surgical approach permits assessing the characteristics of the bony lesion and those of the affected area’. This statement was written by Fermin A. Carranza Sr. as the introduction to his Doctoral Thesis ‘Surgical Treatment of Paradentosis (Alveolar Phyorrea)’ approved at the Medical School, National University of Buenos Aires, Argentina, and published in 1935 (7). The truth is that Latin American dentists have been pioneers in the field of periodontology. Although their early communications were devoted to the nonsurgical treatment of periodontitis, it was Carranza Sr. who pioneered the development of the knowledge of periodontics in Argentina and Latin America. Following Neumann’s publications, Carranza Sr. began treating periodontal disease using the flap approach and, in 1928, published his first article related to the surgical treatment of ‘alveolar pyorrhea’ (6). In 1942, a few years after completing his doctoral thesis, he published his classical article ‘When and why bone should be sacrificed in the treatment of Paradentosis’ (5). In this article he presented drawings and cases for which he recommended removal of alveolar bone. Those indications were very similar, and in certain cases identical, to those published by Schluger in his classical publication of 1949 (22). The language barrier and the geographical distance contributed to the lack of communication between those two researchers. Aside from his interest in the clinical area, and being a devoted clinician, Carranza Sr. worked closely with his thesis mentor, Rodolfo Erausquin, who was
an eminent oral pathologist. Together they studied autopsy specimens to describe the histopathology of periodontal diseases (2, 3, 8, 10). These studies constituted the basis for their understanding of the periodontal disease process and for Carranza’s future approach to treatment and his emphasis on ‘reattachment’ in publications many years later. Carranza’s influence transcended the early developments of the periodontal discipline and the boundaries of Latin America. He lectured extensively in Argentina and in other Latin American countries, as well as in Europe and the USA. Carranza Sr. formed a large group of followers, who became leaders in the field of periodontics. The strong development of periodontics in Argentina was not an isolated event. At the same time, across the Andes, in Chile, another group was promoting the development of periodontics. In 1924, at the School of Biological and Medical Sciences at the University of Chile in Santiago, a ‘Department of Parodontics’ was established. This was probably one of the first, if not the first, department in the world solely devoted to periodontal teaching. Alfonso Leng was in charge, and in 1932 was appointed Full Professor of Parodontics. Juan Villavicencio Rubio joined him in 1926. When the School of Dentistry was established, both continued to be responsible for the teaching of periodontics at all different levels and carried on research until their retirement from academia. Simultaneously, in Uruguay, a neighboring state of Argentina, other individuals were also devoting their professional career to periodontics, of whom Francisco M. Pucci and Jorge Mazzoni were the leaders (17, 18, 20). In 1940, Francisco M. Pucci published ‘Paradencio – Patologia y Tratamiento’, a comprehensive treatise with several editions, almost 700 pages long and wholly dedicated to periodontics, which for many years was the leading such text in Latin America (19).
7
Caffesse
The interest devoted to periodontics in the southern part of Latin America spread, over time, to other countries in the region. Pedro Ayllon (Peru), Focion Febres Cordero and Raul Vincentelli (Venezuela), Guillermo Gamboa, Rafael Lozano and Antonio Ruiz (Mexico), Cesio de Padua Lima and Rugerpe A. Pedre~ o, Jose Rezk and ira (Brazil) and Guillermo London Carlos de Castro (Colombia), among many others, represented the nuclei of individuals in their own countries who were educating the dental profession on the importance of periodontics for oral and systemic health. However, it is undisputable that the trio of Fermin A. Carranza Sr., Alfonso Leng and Francisco M. Pucci constitute the historic core who greatly influenced all Latin America and beyond, and that these individuals were responsible for the high level of development and consideration that periodontics has gained within dentistry in that part of the world.
Current periodontics The scope of current periodontics in Latin America is, of course, quite different from that of the early decades of the last century. Education, research and clinical practice have evolved, a formal postgraduate program in periodontics has been established in many universities of Latin America and many individuals have traveled to US and European universities to complete their formal training, including research. Fortunately, many have returned to their home countries and have continued their academic and investigative activities with some financial support from governments. Consequently, the volume of presentday research in periodontics from Latin America is significant and thus selecting the topics and contributors for this volume of Periodontology 2000 was difficult. The papers included here represent only a small sample of the myriad of periodontal research that is taking place throughout Latin America. The prevalence and the severity of periodontal diseases in Latin America have been topics of research for many years; however, even today we do not have a clear understanding of the magnitude of these diseases throughout the continent. Oppermann et al. (15) report on the epidemiology of adult periodontal diseases, and Botero et al. (4) report on the epidemiology of periodontal diseases in children and adolescents. Both articles point out the heterogeneity of the studies performed, most of which are cross-sectional, with methodologies and periodontal assessment indices that are difficult to compare. In spite of the
8
difficulties, it is clear that the prevalence of periodontal disease is very high in Latin America and it relates to all the known risk factors for the disease. Some demographic factors assume particularly great importance for periodontal disease in Latin America. There exist marked variations in race and ethnicity within and among the countries, and there are significant disparities among the populations in terms of education and socio-economic status, with more than half of the population living below the poverty line with minimal access to dental care. In general, the percentage of periodontally healthy subjects decreases with age, along with an increase in plaque and calculus accumulation. Periodontitis increases with age and is more prevalent in male subjects, heavy smokers and individuals of low socio-economic status. A 5-year longitudinal epidemiological study from Brazil estimated an average loss of attachment of 0.33 mm/ year at the worst interdental site of each tooth and of 0.10 mm/year at the remaining four interdental sites per tooth. These values fall midway between those reported for populations with minimal dental care and those reported for well-maintained populations. Botero et al. (4) have reviewed periodontal diseases in children and adolescents and found a scarcity of periodontal studies of young people in Latin America. Gingivitis is prevalent in children and adolescents, but other manifestations of periodontal disease can also be found, including aggressive periodontitis, acute necrotizing ulcerative gingivitis and herpesvirus and fungal infections. The overall mean prevalence of gingivitis in Latin America is reported to be 34.7%, varying among individual countries from 24 to 77%. The prevalence of bleeding on probing is reported to be 15–35%. Aggressive periodontitis in adolescents is approximately 2% and incipient periodontitis is 20%. Acute necrotizing ulcerative gingivitis and necrotizing ulcerative periodontitis, leading to noma/cancrum oris, have been documented in children in Colombia, who had predisposing factors such as acute herpetic gingivostomatitis or measles, combined with malnutrition and poor oral hygiene. The high prevalence of gingivitis and its possible progression to periodontitis stresses the importance of early diagnosis and treatment, and the need for public campaigns to educate the population about the benefits of controlling gingivitis at an early age. The inter-relationship between biofilm microorganisms and the host response has attracted a significant amount of research globally, including Latin America. Contreras et al. (9) present an updated review of studies from Latin America on infectious agents in periodontal disease. Owing to the great
Latin American perspective of periodontology
ethnic diversity and challenging economy, people in Latin America may have an elevated risk of acquiring periodontal pathogens and developing periodontal disease. Black people and Mestizos are frequently colonized with Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. The ‘red complex’ bacteria and A. actinomycetemcomitans are closely associated with chronic and aggressive periodontitis, but may show an unequal distribution in different Latin American populations and countries. Other putative periodontal pathogens include gram-negative enteric rods and herpesviruses. Herpes simplex virus type 1, human cytomegalovirus, Epstein–Barr virus and other herpesviruses can be detected in gingival crevicular fluid and within inflamed gingiva, as well as in other areas of the mouth, and have been linked to chronic and aggressive periodontitis and to acute necrotizing ulcerative gingivitis. Hopefully, increased insights into the periodontal microbiota may lead to more affordable periodontal treatments to counteract the almost ‘epidemic’ nature of destructive periodontal disease in low-income individuals of Latin America. The relationship between periodontal diseases and systemic conditions has been a topic of research onand-off for the past century. Systemic conditions can affect the prevalence and progression of periodontitis, but, at the same time, periodontitis may be a significant risk factor for several systemic conditions, including cardiovascular diseases, stroke, low birth weight and preterm birth, diabetes, osteoporosis, chronic obstructive pulmonary disease and pneumo pez et al. (12) address the effects of periodonnia. Lo tal disease on preterm birth rate. Although several papers have been written on this association, and intervention studies have been performed, the reported results are controversial and published systematic reviews and meta-analyses have not helped to clarify the issue. The methodological aspects of the individual randomized clinical trials included in the meta-analyses, may not have clearly determined and controlled inclusion and exclusion criteria, periodontal disease status, confounding factors for preterm birth, the periodontal effectiveness of intervention regimes, and specific end-points as thera pez et al. (12) have evaluated peutic outcomes. Lo the conclusion of six meta-analyses, four of which found no effect and two of which did find an effect of periodontal treatment on preterm birth rate. pez et al. (12) suggest that trials with a proper defLo inition of periodontitis, including probing pocket depth and clinical attachment level, and effective control of periodontal infections have indeed
demonstrated a reduced rate of preterm birth following periodontal therapy. The use of systemic antibiotics in periodontal treatment has been a topic of controversy. Feres et al. (11) present a comprehensive review, emphasizing their own clinical and microbiological research, including randomized clinical trials of 1–2 years’ duration. They stress the ecological concept that the entire mouth ought to be regarded as a unit of bacteria living in biofilm accumulations. That notion supports the use of systemic, rather than local, antibiotic therapy for the control of pathogenic bacteria residing in different sites of the oral cavity. One of the main concerns with the use of systemic antibiotics has been the development of bacterial resistance; however, according to their research, resistance is only transient, and by 3 months bacterial-sensitivity patterns return to baseline values. The authors stress the importance of combating the ‘red complex’ pathogens and A. actinomycetemcomitans, as well as other newly recognized microbial species, in periodontal disease. Based on randomized clinical trials designed to evaluate the clinical and microbiological effects of various systemic antibiotics, Feres et al. (11) conclude that young individuals with aggressive periodontitis and adults with generalized chronic periodontitis can benefit from a 14-day treatment with amoxicillin plus metronidazole combined with local mechanical therapy. However, that treatment seems to be less effective in smokers because of an inadequate response of the ‘orange complex’ bacteria, which serve as precursors for the colonization of the major pathogenic bacteria of the ‘red complex’. A failure of periodontal therapy to suppress the periodontopathic microbiota markedly may provide an additional explanation for the reduced treatment response in smokers. Feres et al. (11) utilize their reported data to support and promote the use of systemic antibiotics during the active phase of periodontal therapy. Smoking comprises a very significant risk factor for the overall health of an individual, although it is one of the lifestyles that can be modified. The prevalence of smoking in Latin America is not well established, but is estimated to be in the magnitude of 8–10%, and is particularly widespread in populations of low socio-economic and educational standing. Female subjects in Latin America seem to smoke more than female subjects in the rest of the world, and the habit begins in adolescence. Another significant problem is passive smoking, both at home and at work – national campaigns promoting smoke-free places have had only limited success and airborne nicotine contamination has been demonstrated in some of the
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important metropolis centers. Nociti et al. (14) present a thorough review on the effect of smoking on periodontal disease, supported by their own in-vitro and in-vivo studies and by other published research. Clinical, microbiological and immunological data are discussed to explain the increased propensity of smokers to experience destructive periodontal disease. Clinically, smokers exhibit more severe loss of alveolar bone, periodontal attachment loss, gingival recession and tooth loss. The number of cigarettes and years of smoking seem to correlate with the progression of periodontitis. Microbiologically, the ‘red complex’ of pathogens and A. actinomycetemcomitans have been identified both in smokers and in nonsmokers; whether the level of these bacteria is different in smokers than in nonsmokers has still to be established. The same pathogens may trigger the production of lower amounts of proinflammatory cytokines, and subsequently relatively little gingivitis, in smokers. The immunological mechanisms of periodontal breakdown in smokers are not clear. Tobacco is cytotoxic, containing potent toxins such as nicotine, carbon monoxide and reactive oxidants that can affect both innate and adaptive immune systems. Therapeutically, smokers show an unfavorable response to nonsurgical and surgical therapy, and to periodontalregenerative and plastic procedures; however, the negative effects of smoking seem to be reversible, with former smokers responding to therapy better than current smokers. Obviously, smoking cessation should constitute a standard part of periodontal therapy. Periodontal regeneration is an important area of research, and significant progress has been made in understanding the cellular and molecular events of regeneration. Periodontal healing and regeneration depends on the availability of proper cells, extracellular matrix or scaffold, and growth and differentiation factors. Research on periodontal regeneration in Latin America has involved cementoblasts, growth factors and mesenchymal stem cells. The article by Arzate et al. (1) evaluates the role of cementum molecules in the formation, repair and regeneration of the periodontium. The authors review collagen and noncollagen proteins of cementum, and describe in detail the cementum protein type 1, which is responsible for 70% of the mitogenic activity in cementum. Cementum protein type 1 is expressed in human gingival fibroblasts and periodontal ligament cells, is released during demineralization and repair, and seems to regulate the growth and composition of apatite crystals. The enamel-associated proteins amelogenin and enamelin are also found in cementum and may be involved in acellular cementum formation.
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Smith et al. (23) address the topic of growth factors and cytokines and their ability to bind to cell receptors, activate transmembrane signaling and trigger the orderly sequence of intracellular responses involved in periodontal healing. Smith et al. (23) discuss growth factors associated with periodontal healing and regeneration, including transforming growth factor-beta, platelet-derived growth factor and bone morphogenetic proteins. Transforming growth factorbeta supports extracellular matrix deposition and remodeling during wound healing. Platelet-derived growth factor stimulates cell proliferation and chemotaxis, and is believed to be involved in the initial stages of healing. Bone morphogenetic proteins belong to the transforming growth factor-beta superfamily and participate in cartilage and bone formation, remodeling and repair. Sanz et al. (21) discuss the use of mesenchymal stem cells from the oral cavity in tissue regeneration. Oral stem cells are present in the pulp tissue of permanent teeth. The pulpal stem cells can differentiate into odontoblasts, osteoblasts, chondrocytes, adipocytes, neurocytes and pluripotent stem cells, and have the potential to develop dentin/pulp complexes. Stem cells isolated from the apical papilla of developing teeth can differentiate into chondrogenic, osteogenic or adipogenic lineages, display dentinogenic markers and induce root formation. Stem cells from the periodontal ligament can differentiate into cementoblasts. Finally, stem cells are present in gingival connective tissue. Gingivalderived stem cells are readily harvested and can differentiate into osteogenic, chondrogenic and adipogenic lineages. The approaches to tissue regeneration presented above may one day lead to the development of effective and reproducible regenerative therapies in periodontics. Lasers have been used in periodontics since their introduction in the medical field. When used in surgery, lasers may increase blood flow and promote cell proliferation and healing by recruiting cytokines and growth factors to the wound. Passanezi et al. (16) review current concepts and uses of high- and lowintensity lasers in periodontal therapy, mainly based on findings reported by Latin American researchers. High-intensity lasers have been used in nonsurgical periodontal therapy for root biomodification and in the treatment of root hypersensitivity, and low-intensity lasers have been used to improve regenerative procedures and in antimicrobial photodynamic therapy. However, the use of laser treatment in periodontics is surrounded by controversy regarding the real clinical benefits, as the research results are conflicting and difficult to extrapolate to clinical practice. Con-
Latin American perspective of periodontology
tributing to the confusion is research reports of laser units with different wavelength and irradiation settings, which are important determinants of the clinical outcome. Nonetheless, laser treatment seems to have great patient acceptance and may be applied to individuals who object to or are recalcitrant to traditional periodontal therapy, as in diabetic, immunocompromised or disabled patients. Basic and clinical research in areas that may be peripheral, but still have significance and interest for periodontics, is also underway in Latin America. Monti-Hughes et al. (13) report on research being conducted on ‘field cancerization’ using the hamster cheek pouch model. Field cancerization refers to the changes that carcinogens, such as tobacco and alcohol, can induce in the oral mucosa, producing molecular changes that can be detected by histochemical techniques in biopsies, before histological modifications can be identified. Carcinogens applied in solution on the mucosal surface of the hamster cheek pouch induce alterations mimicking those detected in the human oral mucosa. The hamster model has also been proposed and validated for testing Boron Neutron Capture Therapy, a novel approach in the treatment of oral cancer, and clinical trials are already underway for certain tumor types and localizations. Boron Neutron Capture Therapy has been proposed as a more selective and effective approach in the treatment of head and neck cancer. The therapy administers boron carriers, which are taken up primarily by neoplastic cells, followed by irradiation with a neutron beam. The hamster cheek pouch model was also adapted for long-term studies of field cancerization, and the authors were able to show the inhibitory effect of Boron Neutron Capture Therapy on the development of tumors in field cancerized tissues, with acceptable levels of slight mucositis as a dose-limiting side-effect. In conclusion, this volume of Periodontology 2000 reviews the epidemiology, the etiopathology and the treatment of periodontal diseases in Latin America. Emphasis is placed on the microbiology of periodontitis, the effect of smoking and the benefits of systemic antibiotics and laser treatment. In addition, basic research in new areas of regeneration and in cancer therapy is also presented. The present volume of Periodontology 2000 is a vivid representation of the variety and the high quality of research that is carried out in laboratories, institutes and universities throughout Latin America. Latin America faces the same periodontal-disease concerns as in other parts of the world, but also has to confront unique challenges in a large
population of socio-economically disadvantaged individuals who receive little or no periodontal healthcare. The articles presented here will hopefully stimulate further studies on periodontal disease prevention and treatment to help combat the high level of edentulism in Latin America.
Acknowledgments Appreciation is expressed to the following colleagues and friends who helped with historical information: Drs Fermın A. Carranza Jr., Mauricio Echeverri, Ernesto Muller, Antonio W. Sallum, Juan J. Villavicencio n. R and Agustın Zero
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n FS, Chaparro AP. Mesenchymal stem cells 21. Sanz AR, Carrio from the oral cavity and their potential value in tissue engineering. Periodontol 2000 2015: 67: 251–267. 22. Schluger S. Osseous resection – A basic principle in periodontal surgery. Oral Surg Oral Med Oral Pathol 1949: 2: 316–325. ceres M, Martınez J. Research in 23. Smith PC, Martınez C, Ca growth factors in periodontology. Periodontol 2000 2015: 67: 234–250.
