Subjects harboring HIV show poor clinical periodontal condition and higher prevalence of Porphyromonas gingivalis and  Tannerella forsythia

Guimarães, Gustavo; Guimarães, G. C. N.; Cortelli, José Roberto; Cogo, Karina; Costa, Fernando Oliveira; Aquino, Davi Romeiro; Lustosa, Alexandre; Cortelli, Sheila Cavalca

Original Article

Subjects harboring HIV show poor clinical periodontal condition and higher prevalence of Porphyromonas gingivalis and Tannerella forsythia

Portadores do HIV apresentam pior condição clínica periodontal e maior prevalência de Porphyromonas gingivalis e Tannerella forsythia

Guimarães, Gustavo; Guimarães, G. C. N.; Cortelli, José Roberto; Cogo, Karina; Costa, Fernando Oliveira; Aquino, Davi Romeiro; Lustosa, Alexandre; Cortelli, Sheila Cavalca

Rev. odontol. UNESP, vol.41, n1, p.15-21, 2012

PDF

Downloads: 1

Abstract

Objective: This cross-sectional study aimed at understanding whether clinical features and frequency of the periodontal pathogens Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia and Treponema denticola differ in periodontitis subjects infected with HIV when compared to non-infected subjects. Material and method: 35 periodontitis subjects were selected for the HIV+ group and 35 for the HIV-group; both groups were matched according to age, gender and a site-based criterion to determine periodontal disease. In a second visit, clinical periodontal status of the whole mouth of each participant was determined by plaque index (PI), gingival index (GI) bleeding on probing index (BOP), probing depth (PD) and clinical attachment level (CAL) measurements. The frequency of P. gingivalis, A. actinomycetemcomitans, T. forsythia and T. denticola was assessed by polymerase chain reaction (PCR) from unstimulated saliva samples. Statistical analysis was performed using the Mann Whitney, Student-t and Chi-Square tests (p<0,05). Result: Despite screening through a specific selection criterion, HIV+ subjects showed more periodontal breakdown, demonstrated by higher mean values of PD, CAL (p<0.05, Student-t test), PI, GI, BOP (p < 0, 05, Mann Whitney test) in comparison to HIV- controls. Also, a higher number of HIV+ subjects harbored two of the searched species: P. gingivalis (p = 0.0007, chisquare) and T. forsythia (p = 0.0001, Chi-square). Conclusion: HIV+ patients had poorer periodontal status and a higher prevalence of P. gingivalis and T. forsythia, two red complex bacterial species, which are clearly associated with damaged periodontal tissues.

Keywords

Acquired immunodeficiency syndrome, microbiology, bacteria, periodontitis.

Resumo

Objetivo: O presente estudo transversal objetivou entender se os aspectos clínicos periodontais e a frequência dos patógenos periodontais Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia diferem em pacientes periodontais infectados pelo HIV comparativamente a indivíduos não infectados pelo vírus. Material e método: Foram selecionados para o estudo indivíduos com periodontite sendo 35 HIV+ e 35 HIV-; ambos os grupos foram pareados quanto a idade, gênero e um critério sítio-dependente de determinação de doença periodontal. Em visita subsequente, o exame periodontal completo determinou a condição periodontal geral dos indivíduos pelas mensurações do índice de placa (IP), índice gengival (IG), índice de sangramento à sondagem (ISS), profundidade de sondagem (PS) e nível de inserção clínica (NIC). A frequência das espécies bacterianas foi avaliada por meio de reação de polimerase em cadeia (PCR) — a partir de amostras obtidas da saliva não estimulada. A análise estatística foi realizada por meio dos testes Mann-Whitney, t de Student e Qui-quadrado (p<0,05). Resultado: Apesar da triagem através de critério especifico de seleção, indivíduos HIV+ apresentaram maior destruição periodontal revelada pelas maiores médias de PS, NIC (p<0,05, t de Student), IP, IG, ISS (p<0,05, Mann Whitney). Além disso, um maior número de indivíduos HIV+ alocaram duas das espécies pesquisadas: P. gingivalis (p= 0,0007, Qui-Quadrado) e T. forsythia (p= 0,0001, Qui-Quadrado). Conclusão: Indivíduos HIV+ apresentaram pior condição periodontal e frequência mais elevada de P. gingivalis e T. forsythia, espécies do complexo vermelho que estão claramente associadas a tecidos periodontais danificados.

Palavras-chave

Síndrome de Imunodeficiência Adquirida, microbiologia, bactérias, periodontite.

References

1. Mataftsi M, Skoura L, Sakellari D. HIV infection and periodontal diseases: an overview of the post-HAART era. Oral Dis 2011; 17:13-25. PMid:21029260. http://dx.doi.org/10.1111/j.1601-0825.2010.01727.x

2. Bhayat A, Yengopal V, Rudolph MJ, Nemutandani MS. Predicting HIV in a public dental facility using group I oral lesions. SADJ. 2008; 63:538-43. PMid:19322964.

3. Shangase L, Feller L, Blignaut E. Necrotising ulcerative gingivitis/periodontitis as indicators of HIV-infection. SADJ. 2004; 59:105-8. PMid:15214212.

4. Tomar SL. Loss of periodontal attachment in HIV-seropositive military personnel. J Periodontol. 1995; 66:421-8. PMid:7562330. http:// dx.doi.org/10.1902/jop.1995.66.6.421

5. Coogan MM, Greenspan J, Challacombe SJ. Oral lesions in infection with human immunodeficiency virus. Bull World Health Organ. 2005; 83:700-6. PMid:16211162. PMCid:2626330.

6. Lucht E, Helmdahl A, Nord CE. Periodontal disease in HIV-infected patients in relation to lymphocyte subsets and specific microorganisms. J Clin Periodontol. 1991;18:252-6. PMid:1677365. http://dx.doi.org/10.1111/j.1600-051X.1991.tb00423.x

7. Alves M, Mulligan R, Passaro D, Gawelll S, Navazesh M, Phelan J, et al. Longitudinal evaluation of loss of attachment in HIV-infected women compared to HIV-uninfected women. J Periodontol. 2006; 77: 773-9. PMid:16671868. http://dx.doi.org/10.1902/jop.2006.P04039

8. Ranganathan K, Magesh KT, Kumarasamy N, Solomon S, Viswanathan R, Johnson NW. Greater severity and extent of periodontal breakdown in 136 south Indian human immunodeficiency virus seropositive patients than in normal controls: a comparative study using community periodontal index of treatment needs. Indian J Dent Res. 2007; 18(2): 55-9. PMid:17502708. http://dx.doi.org/10.4103/0970- 9290.32420

9. Teanpaisan R, Douglas CW, Nittayananta W. Isolation and genotyping of black-pigmented anaerobes from periodontal sites of HIV‑positive and non-infected subjects in Thailand. J Clin Periodontol. 2001; 28: 311-8. PMid:11314886. http://dx.doi.org/10.1034/ j.1600-051x.2001.028004311.x

10. Doshi D, Ramapuram J, Anup N. Periodontal status of HIV-positive patients. Med Oral Patol Oral Cir Bucal. 2009; 14: e384-e387. PMid:19415052.

11. Murray PA, Grassi M, Winkler JR. The microbiology of HIV-associated periodontal lesions. J Clin Periodontol. 1989; 16: 636-42. PMid:2693496. http://dx.doi.org/10.1111/j.1600-051X.1989.tb01032.x

12. Cross KD, Smith GL. Comparison of periodontal disease in HIV seropositive subjecs and controls (II). Microbiology, immunology and predictors of disease progression. J Clin Periodontol. 1995; 22: 569-77. PMid:7560241. http://dx.doi.org/10.1111/j.1600-051X.1995. tb00806.x

13. Alpagot T, Duzqunes N, Wolff LF, Lee A. Risk factors for periodontitis in HIV patients. J Periodontal Res. 2004; 39: 149-57. PMid:15102043. http://dx.doi.org/10.1111/j.1600-0765.2004.00718.x

14. Nakou M, Kamma J, Gargalianos P, Laskaris G, Mitsis F. Periodontal microflora of HIV infected patients with periodontitis. Anaerobe. 1997; 3: 97-102. PMid:16887570. http://dx.doi.org/10.1006/anae.1997.0081

15. Patel M, Coogan M, Galpin JS. Periodontal pathogens in subgingival plaque of HIV-positive subjects with chronic periodontitis. Oral Microbiol Immunol. 2003;18:199-201. PMid:12753474. http://dx.doi.org/10.1034/j.1399-302X.2003.00064.x

16. Gonçalves LS, Soares Ferreira SM, Souza CO, Souto R, Colombo AP. Clinical and microbiological profiles of human immunodeficiency virus (HIV)-seropositive Brazilians undergoing highly active antiretroviral therapy and HIV-seronegative Brazilians with chronic periodontitis. J Periodontol. 2007; 78: 87-96. PMid:17199544. http://dx.doi.org/10.1902/jop.2007.060040

17. Associação Brasileira das Empresas de Pesquisa (ABEP). Critério de Classificação Econômica Brasil [citado em 2007 Set. 11]. Disponível em: http://www.abep.org/novo/CMS/Utils/FileGenerate.ashx?id=46.

18. Center for Diseases Control and Prevention (CDC). Revised Surveillance Case Definitions for HIV Infection Among Adults, Adolescents, and Children Aged <18 Months and for HIV Infection and AIDS Among Children Aged 18 Months to <13 Years --- United States, 2008. MMWR. 2008; 57(RR10);1-8. Disponível em: http://www.cdc.gov/mmwr/preview/mmwrhtml/rr5710a1.htm?s_cid=rr5710a1_e#top

19. López NJ, Smith PC, Gutierrez J. Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res. 2002; 81: 58-63. PMid:11820369. http://dx.doi.org/10.1177/154405910208100113

20. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between bucal hygiene and periodontal condition. Acta Odontol Scand. 1964; 22: 112-35. PMid:14158464. http://dx.doi.org/10.3109/00016356408993968

21. Cortelli SC, Cortelli JR, Holzhausen M, Franco GC, Rebelo RZ, Sonagere AS, et al. Essential oils in one-stage full-mouth disinfection: double-blind, randomized clinical trial of long-term clinical, microbial and salivary effects. J Clin Periodontol. 2009; 36:.333-42.

22. Alpagot T, Remien J, Bhattacharyya M, Konopka K, Lundergan W, Duzgunes N. Longitudinal evaluation of prostaglandin E2 (PGE2) and periodontal status in HIV+ patients. Arch Oral Biol. 2007; 52: 1102-8. PMid:17586460. PMCid:2083300. http://dx.doi.org/10.1016/j. archoralbio.2007.04.013

23. Kroidl A, Schaeben A, Oette M, Wsttstein M, Herfordt A, Häussinger D. Prevalence of oral lesions and periodontal diseases in HIV‑infected patients on antiretroviral therapy. Eur J Med Res. 2005; 10:448-53. PMid:16287607.

24. Gonçalves LS, Ferreira SM, Souza CO, Colombo AP. Influence ofIL-1 gene polymorphism on the periodontal microbiota of HIV-infected Brazilian individuals. Braz Oral Res. 2009; 23: 452-9. http://dx.doi.org/10.1590/S1806-83242009000400016

25. Guthmiller JM, Lally ET, Korostoff J. Beyond the specific plaque hypothesis: are highly leukotoxic strains of actinobacillus actinomycetemcomitans a paradigm for periodontal pathogenesis? Crit Rev Oral Biol Med. 2001; 12: 116-24. http://dx.doi.org/10.1177/ 10454411010120020201

26. Tanabe SI, Bodet C, Grenier D. Treponema denticola peptidoglycan induces the production of inflammatory mediators and matrix metalloproteinase 9 in macrophage-like cells. J Periodontal Res. 2008; 44: 503-10. PMid:18973520. http://dx.doi.org/10.1111/j.1600- 0765.2008.01141.x

27. Tenenbaum H, Elkaim R, Cuisinier F, Dahan M, Zamanian P, Lang JM. Prevalence of six periodontal pathogens detected by DNA probe method in HIV vs non-HIV periodontitis. Oral Dis. 1997; 3 Suppl 1: S153-5. PMid:9456680.

28. Brito A, Escalona LA, Correnti M, Perrone M, Bravo IM, Tovar V. Periodontal conditions and distribution of Prevotella intermedia, Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans in HIV-infected patients undergoing anti-retroviral therapy and in an HIV-seronegative group of the Venezuelan population. Acta Odontol Latinoam. 2008; 2 (1): 89-96.

29. Imai K, Ochiai K, Okamoto T. Reactivation of latent HIV-1 infection by the periodontopathic bacterium Porphyromas gingivalis involves histone modification. J Immunol. 2009; 15: 2688-95.

30. Huang CB, Alimova YV, Ebersole JL. HIV-1 reactivation in HIV-latently infected dentritic cells by oral microorganisms and LPS. Cell Immunol. 2011; 268:105-11. PMid:21420664. http://dx.doi.org/10.1016/j.cellimm.2011.02.003