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Most common oral manifestations in pediatric patients HIV positive and the effect of highly active antiretroviral therapy

Abstract

This integrative literature review aims to identify the main oral lesions affecting pediatric patients with HIV, and describe the effect of highly active antiretroviral therapy (HAART) on these injuries, comparing it to antiretroviral therapy (ART). A search was conducted in PubMed and Scielo databases, following predetermined inclusion and exclusion criteria. 19 papers were selected and the main information on the prevalence and frequency of oral manifestations in HIV-positive pediatric patients and effect of therapy applied were extracted. The most frequent injuries were oral candidiasis, gingivitis, parotid gland enlargement and linear gingival erythema. The use of HAART shown to reduce the prevalence of oral manifestations in pediatric patients with HIV and be more effective than ART. The findings of this study suggest that the most frequent oral manifestation in HIV-infected children is oral candidiasis, followed by changes such as gingivitis and enlargement parotid glands. The use of HAART appears to reduce the prevalence of these oral lesions, showing more effective results than ART.

Key words
Child; Acquired Immunodeficiency Syndrome; Oral manifestations; Antiretroviral therapy

Resumo

Esta revisão integrativa da literatura tem por objetivo identificar as principais lesões bucais que afetam pacientes pediátricos com HIV, bem como descrever o efeito da terapia antirretroviral altamente ativa (HAART) sobre essas lesões, comparando-a com a terapia antirretroviral (ART). Foi feita uma busca nas bases de dados PubMed e Scielo, seguindo critérios de inclusão e exclusão pré-determinados. Foram selecionados dezenove artigos científicos e extraídas as informações principais sobre prevalência e a frequência das manifestações bucais em pacientes pediátricos HIV positivos e o efeito da terapêutica aplicada. As lesões mais frequentes foram candidíase oral, gengivite, aumento das parótidas e eritema gengival linear. O uso da HAART mostrou diminuir a prevalência das manifestações bucais nos pacientes pediátricos com HIV e ser mais eficaz que a ART. Os achados deste estudo sugerem que a manifestação bucal mais frequente em pacientes pediátricos com HIV é a candidíase oral, seguida de alterações como gengivite e aumento das glândulas parótidas. O uso de HAART parece reduzir a prevalência dessas lesões orais, apresentando resultados mais eficazes que os da ART.

Palavras-chave
Criança; Síndrome de imunodeficiência adquirida; Manifestações bucais; Terapia antirretroviral

Introduction

Acquired Immunodeficiency Syndrome (AIDS) is a systemic disease caused by the Human Immunodeficiency Virus (HIV), which affects the individual's immune system and makes him/her more susceptible to other diseases of systemic origin, such as oral lesions11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372..

First cases of AIDS were reported in the mid-1980s and its heterosexual transmission has grown over time, affecting a large number of women of childbearing age and capable of transmitting HIV virus to their children22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.. This vertical transmission, from mother to child, is considered the main factor for the increasing prevalence of this disease in pediatric patients22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.44. Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271. and it can occur during pregnancy, childbirth or through breastfeeding55. Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.,66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505..

HIV infection currently affects more than 2 million children under the age of 15 years old worldwide and it is associated with numerous life-long comorbidities for this population66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505.,77. Domaneschi C, Massarente DB, de Freitas RS, Sousa Marques HH, Paula CR, Migliari DA, Antunes JL. Oral colonization by Candida species in AIDS pediatric patients. Oral Dis 2011; 17(4):393-398.. Early identification of oral manifestations, which usually are the first signs of this infection or its progression in children22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61., may assist in choosing appropriate therapy and reducing its morbidity66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505..

Immunosupressed patients are more susceptible to opportunistic infections, especially those that affect the oral cavity, such as oral candidiasis88. Konstantyner TC, Silva AM, Tanaka LF, Marques HH, Latorre MR. Factors associated with time free of oral candidiasis in children living with HIV/AIDS, São Paulo, Brazil. Cad Saude Publica 2013; 29(11):2197-2207.. This problem becomes worse when it comes to HIV-positive pediatric patients because they present an immature immune system that makes them more prone to severe immunosuppression and rapid disease progression22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.,66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505..

Some oral manifestations in pediatric patients present a different prevalence of adult patients99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.. The prevalence of oral lesions is, on average, 63%11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60., ranging from 20% to 80%1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622.. This variation may occur according to the region or country and type of treatment instituted, such as whether patients have access to more potent antiretroviral drugs44. Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271. or not.

Introduction of antiretroviral therapy (ART) regarding the treatment of HIV-infected patients brought enhancements in their oral health quality of life, reducing frequency of the disease's oral manifestations66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505.. Subsequently, it was created a combination therapy known as highly active antiretroviral therapy (HAART). This one delivered more effective results, altering the prevalence of some oral lesions caused by HIV, besides improving the immune function, which reduced opportunistic infections, morbidity and mortality1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.,1212. Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202..

A wide variety of oral lesions in HIV-infected pediatric patients are reported in the literature, such as: candidiasis88. Konstantyner TC, Silva AM, Tanaka LF, Marques HH, Latorre MR. Factors associated with time free of oral candidiasis in children living with HIV/AIDS, São Paulo, Brazil. Cad Saude Publica 2013; 29(11):2197-2207.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.1212. Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202., gingivitis1212. Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202.1414. Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282., oral hairy leukoplakia99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.,1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071., Kaposi's sarcoma55. Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.,1515. Miziara, ID, Weber R. Oral lesions as predictors of highly active antiretroviral therapy failure in Brazilian HIV infected children. J Oral Pathol Med 2008; 37(2):99-106., parotid enlargement11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,44. Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271.,1414. Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282.,1616. Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146., herpes simplex11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61..This data also reveal divergence of information regarding which ones are the most frequent oral manifestations and how the antiretroviral therapies act on them. For this reason, this present study aims to identify the main oral lesions affecting pediatric patients with HIV, as well as the effects of ART and HAART on said lesions.

Methodology

This integrative review consisted of a bibliographic survey in the PubMed and SciELO databases. Adopting “advanced search” mode, the following keywords were used blended and standalone: “oral manifestations”, “HIV”, “children”, “childhood”, “prevalence”, “HAART”, “antiretroviral therapy” in both Portuguese and English.

Inclusion criteria for the articles were: descriptive, cross-sectional, and comparison studies reporting oral manifestations in HIV-infected children published in Portuguese or English between 2004 and 2014.

After the initial selection, repeated articles were excluded from the sample, along with those which did not include at least three keywords in the title or abstract, were not published in full and did not present the investigated issue as main subject. Last selection step consisted of reading the texts in full, followed by the construction of tables using most relevant information of each selected article.

Results

A total of 367 articles were identified in the databases searched. After excluding duplicate articles and those that did not meet predetermined inclusion and exclusion criteria, there were 24 articles left for full reading. After analyzing the content of each one of them, 19 scientific articles that addressed investigated issues were selected for this review. Most relevant subjects raised were:

  • Identification of oral manifestations affecting HIV-positive pediatric patients, highlighting the most frequent ones;

  • ART and HAART effects on oral lesions of HIV-positive children, especially HAART in the prevalence of these oral manifestations.

Most frequent lesions in HIV-positive pediatric patients were oral candidiasis, gingivitis, parotid enlargement and linear gingival erythema, being oral candidiasis considereda predictor of disease progression. The use of HAART has been shown to decrease the prevalence of oral manifestations in pediatric patients with HIV and to be more effective than ART. Main information contained in each article were described in the form of Charts 1 to 4 and sorted according to their publication year.

Chart 1
Integrative review consolidation.
Chart 2
Integrative review consolidation.
Chart 3
Integrative review consolidation.
Chart 4
Integrative review consolidation.

Discussion

Cross-sectional and prospective studies have shown that pediatric HIV-infected patients will present some type of oral lesion in non-specific phases of their childhood, which will help to identify the correct diagnosis of the syndrome11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.,1717. Kumar RK, Mohan G, Reddy NV, Rao VA, Shameer M, Christopher A. Associated oral lesions in human immunodefeciency virus infected children of age 1 to 14 years in antiretroviral therapy centers in Tamil Nadu. Contemp Clin Dent 2013; 4(4):467-471. and, consequently, to find the most suitableantiretroviral therapy treatment44. Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271.,99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.,1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622..

In all the studies analyzed, although they occurred in different regions and countries, oral manifestations were highlighted as a common feature in children infected with HIV virus. Most commonly found lesions were oral candidiasis in various forms33. Ogunbosi, BO, Oladokun RE, Brown BJ, Osinusi KI. Prevalence and clinical pattern of paediatric HIV infection at the University College Hospital, Ibadan, Nigeria: a prospective cross-sectional study. Ital J Pediatr 2011; 37:29.,77. Domaneschi C, Massarente DB, de Freitas RS, Sousa Marques HH, Paula CR, Migliari DA, Antunes JL. Oral colonization by Candida species in AIDS pediatric patients. Oral Dis 2011; 17(4):393-398.,1414. Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282.,1818. Gaitán-Cepeda LA, Domínguez-Sánchez A, Pavía-Ruz N, Muñoz-Hernández R., Verdugo-Díaz R, Valles-Medina AM, Meráz-Acosta H. Oral lesions in HIV+/AIDS adolescents perinatally infected undergoing HAART. Med Oral Patol Oral Cir Bucal 2010; 15(4):e545-e550., gingivitis22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.,1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071.,1414. Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282.,1616. Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146., acute herpetic gingivostomatitis22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61., linear gingival erythema11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.,1717. Kumar RK, Mohan G, Reddy NV, Rao VA, Shameer M, Christopher A. Associated oral lesions in human immunodefeciency virus infected children of age 1 to 14 years in antiretroviral therapy centers in Tamil Nadu. Contemp Clin Dent 2013; 4(4):467-471., oral hairy leukoplakia55. Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.,99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.,1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071., Kaposi's sarcoma11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,55. Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.,1515. Miziara, ID, Weber R. Oral lesions as predictors of highly active antiretroviral therapy failure in Brazilian HIV infected children. J Oral Pathol Med 2008; 37(2):99-106. and parotid enlargement44. Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271.,1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071.,1515. Miziara, ID, Weber R. Oral lesions as predictors of highly active antiretroviral therapy failure in Brazilian HIV infected children. J Oral Pathol Med 2008; 37(2):99-106.,1919. Meless D, Ba B, Faye M, Diby JS, N'zoré S, Datté S, Diecket L, N'Diaye C, Aka EA, Kouakou K, Ba A, Ekouévi DK, Dabis F, Shiboski C, Arrivé E. Oral lesions among HIV-infected children on antiretroviral treatment in West Africa. Trop Med Int Health 2014; 19(3):246-255.. However, almost all of them reported oral candidiasis as the most frequent manifestation, corroborating with the findings in literature. This fact can be observed in the analysis of Charts 1 to 4 and it will be further discussed in the course of this article.

Regarding periodontal conditions, it can be observed that when it comes to immunosuppressed patients, gingivitis can occur even when the patient is well hygienised and there is no biofilm, which does not happen with healthy children22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61..

In a longitudinal study, Vaseliu et al.1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071. found that gingivitis was the most frequent oral lesion (49%), however, the authors suggest that the relevance of gingivitis in pediatric infection scenario is still unknown. On the other hand, Sowole et al. 1616. Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146. found gingivitis (25.5%) as the second most prevalent lesion, followed by enlargement of parotid glands (3.6%).

Linear gingival erythema has also been described by some authors as a common oral manifestation in these patients11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,1717. Kumar RK, Mohan G, Reddy NV, Rao VA, Shameer M, Christopher A. Associated oral lesions in human immunodefeciency virus infected children of age 1 to 14 years in antiretroviral therapy centers in Tamil Nadu. Contemp Clin Dent 2013; 4(4):467-471., besides also being considered as a unique feature of seropositive patients by Tonelli et al.11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.. These characteristics reinforce the need for a careful clinical evaluation of periodontal condition for a possible early diagnosis ofthe HIV virus’ presence in pediatric patients.

Oral candidias is and its pseudomembranous, angular cheilitis, erythematous and oropharyngeal variants were reported in most studies11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.,22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.,1616. Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146.,1717. Kumar RK, Mohan G, Reddy NV, Rao VA, Shameer M, Christopher A. Associated oral lesions in human immunodefeciency virus infected children of age 1 to 14 years in antiretroviral therapy centers in Tamil Nadu. Contemp Clin Dent 2013; 4(4):467-471.,1919. Meless D, Ba B, Faye M, Diby JS, N'zoré S, Datté S, Diecket L, N'Diaye C, Aka EA, Kouakou K, Ba A, Ekouévi DK, Dabis F, Shiboski C, Arrivé E. Oral lesions among HIV-infected children on antiretroviral treatment in West Africa. Trop Med Int Health 2014; 19(3):246-255.. The first three variants have been described as the types known to be associated with HIV infection nowadays1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622..

Thus, it is possible to affirm that the opportunistic lesion most commonly associated with HIV-infected patients is oral candidiasis and that this finding is fundamental for the early diagnosis of AIDS11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.33. Ogunbosi, BO, Oladokun RE, Brown BJ, Osinusi KI. Prevalence and clinical pattern of paediatric HIV infection at the University College Hospital, Ibadan, Nigeria: a prospective cross-sectional study. Ital J Pediatr 2011; 37:29.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.,1414. Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282.,1616. Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146.,1818. Gaitán-Cepeda LA, Domínguez-Sánchez A, Pavía-Ruz N, Muñoz-Hernández R., Verdugo-Díaz R, Valles-Medina AM, Meráz-Acosta H. Oral lesions in HIV+/AIDS adolescents perinatally infected undergoing HAART. Med Oral Patol Oral Cir Bucal 2010; 15(4):e545-e550.,1919. Meless D, Ba B, Faye M, Diby JS, N'zoré S, Datté S, Diecket L, N'Diaye C, Aka EA, Kouakou K, Ba A, Ekouévi DK, Dabis F, Shiboski C, Arrivé E. Oral lesions among HIV-infected children on antiretroviral treatment in West Africa. Trop Med Int Health 2014; 19(3):246-255.. In addition, this oral manifestation may serve as a marker of disease progression and immunosuppression22. Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.,55. Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.,1313. Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071.,1515. Miziara, ID, Weber R. Oral lesions as predictors of highly active antiretroviral therapy failure in Brazilian HIV infected children. J Oral Pathol Med 2008; 37(2):99-106. since its prevalence is related to lower values of TCD4+ lymphocytes11. Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372..

According to Konstantyner et al.88. Konstantyner TC, Silva AM, Tanaka LF, Marques HH, Latorre MR. Factors associated with time free of oral candidiasis in children living with HIV/AIDS, São Paulo, Brazil. Cad Saude Publica 2013; 29(11):2197-2207., candidias is has a considerable importance in the clinical prognosis of HIV infection, besides being a good indicator to show the non-efficacy of antiretroviral treatment. In their study, antiretroviral therapy (mono, double or triple/highly active) proved to be a significant protective factor against oral manifestations and the latter (triple/highly active) demonstrated a better beneficial effect to prevent candidias is in HIV-positive pediatric patients.

According to Pinheiro et al.1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622., the use of HAART significantly reduces oral manifestations associated with AIDS, because an improvement in the immune systemoccurs and consequently a decrease in the incidence and prevalence of opportunistic infections. Such finding was reported in other studies that compared oral manifestations in HIV-positive children with or without the use of this therapy, where those who received the medication had a lower prevalence of oral disorders than children who did not receive said treatment99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.,1010. Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.,1212. Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202..

Corroborating with the affirmative protective action of antiretroviral drugs, Meless et al.1919. Meless D, Ba B, Faye M, Diby JS, N'zoré S, Datté S, Diecket L, N'Diaye C, Aka EA, Kouakou K, Ba A, Ekouévi DK, Dabis F, Shiboski C, Arrivé E. Oral lesions among HIV-infected children on antiretroviral treatment in West Africa. Trop Med Int Health 2014; 19(3):246-255. observed in their study a low prevalence of oral lesions, possibly because all the children in the study were being treated with this type of medication. Jose et al.66. Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505. compared patients that used and did not use HAART and observed that those on this medication had oral manifestations with moderate intensity, with a lower occurrence of oral candidiasis. In addition, there was a significant reduction in the presence oflesions when the treatment time with HAART was longer, especially in periods that exceed five months.

Ogumbosi et al.33. Ogunbosi, BO, Oladokun RE, Brown BJ, Osinusi KI. Prevalence and clinical pattern of paediatric HIV infection at the University College Hospital, Ibadan, Nigeria: a prospective cross-sectional study. Ital J Pediatr 2011; 37:29. study showed that the high number of deaths was related to pre-antiretroviral era and that lower mortality rates were observed when ART was instituted. On the other hand, Ponnamet al.1212. Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202. observed that the administration of HAART increased thedisease's free time, with a consequent raise in patients’ survival rates. However, it is important to point out that unusual clinical manifestations of oral lesions may appear due to the immune response restoration, known as immune reconstitution syndrome (IRS). This may occur a few weeks after starting the treatment1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622. and professionals involved should watch out for this adverse effect.

It is important to highlight that the use of HAART may be associated with a lower prevalence of oral lesions compared to the use of ART99. Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.. Therefore, it is possible to say that HAART plays a key role in reducing the prevalence of oral manifestations in HIV-positive pediatric patients, contributing substantially to give saidimmunosuppressed patients a better quality of life1111. Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622.,1818. Gaitán-Cepeda LA, Domínguez-Sánchez A, Pavía-Ruz N, Muñoz-Hernández R., Verdugo-Díaz R, Valles-Medina AM, Meráz-Acosta H. Oral lesions in HIV+/AIDS adolescents perinatally infected undergoing HAART. Med Oral Patol Oral Cir Bucal 2010; 15(4):e545-e550..

Final Considerations

The findings of this study suggest that the most frequent oral manifestation in HIV-infected children is oral candidiasis, followed by alterations such as gingivitis and parotid glandsenlargement, being candidiasis regarded as a marker of disease progression. It is relevant to point out that oral manifestations are common in seropositive pediatric patients and treating them is fundamental to improve these children quality of life. In addition, HAART seems to reduce the prevalence of said oral lesions, making its use beneficial for patients.

Referências

  • 1
    Tonelli SQ, Oliveira WF, Oliveira GA, Popoff DAV, Coelho MQ, Barbosa Júnior ES. Manifestações bucais em pacientes pediátricos infectados pelo HIV: uma revisão sistemática da literatura. RFO 2013; 18(3):365-372.
  • 2
    Rosendo IA, Ferreira SMS, Pugliesi DM. Avaliação das condições bucais em crianças infectadas pelo HIV atendidas em um posto de assistência municipal de Maceió-AL. Estudo longitudinal. Revista Semente 2011; 6(6):53-61.
  • 3
    Ogunbosi, BO, Oladokun RE, Brown BJ, Osinusi KI. Prevalence and clinical pattern of paediatric HIV infection at the University College Hospital, Ibadan, Nigeria: a prospective cross-sectional study. Ital J Pediatr 2011; 37:29.
  • 4
    Glick M. Orofacial disorders in children with HIV disease. Dent Clin N Am 2005; 49(1):259-271.
  • 5
    Leao JC, Ribeiro CM, Carvalho AA, Frezzini C, Porter S. Oral complications of HIV disease. Clinics (Sao Paulo) 2009; 64(5):459-470.
  • 6
    Jose R, Chandra S, Puttabuddi JH, Vellappally S, Al Khuraif AA, Halawany HS, Abraham NB, Jacob V, Hashim M. Prevalence of oral and systemic manifestations in pediatric HIV cohorts with and without drug therapy. Curr HIV Res 2013; 11(6):498-505.
  • 7
    Domaneschi C, Massarente DB, de Freitas RS, Sousa Marques HH, Paula CR, Migliari DA, Antunes JL. Oral colonization by Candida species in AIDS pediatric patients. Oral Dis 2011; 17(4):393-398.
  • 8
    Konstantyner TC, Silva AM, Tanaka LF, Marques HH, Latorre MR. Factors associated with time free of oral candidiasis in children living with HIV/AIDS, São Paulo, Brazil. Cad Saude Publica 2013; 29(11):2197-2207.
  • 9
    Miziara ID, Filho BC, Weber R. Oral lesions in Brazilian HIV infected children undergoing HAART. Int J Pediatr Otorhinolaryngol 2006; 70(6):1089-1096.
  • 10
    Sales-Peres SHC, Mapengo MA, Moura-Grec PG, Marsicano JA, Sales-Peres AC, Sales-Peres A. Oral manifestations in HIV+ children in Mozambique. Cien Saude Colet 2012; 17(1):55-60.
  • 11
    Pinheiro RS, França TT, Ribeiro CMB, Leão JC, Souza IPR, Castro GF. Oral manifestations in human immunodeficiency virus infected children in highly active antiretroviral therapy era. J Oral Pathol Med 2009; 38(8):613-622.
  • 12
    Ponnam SR, Srivastava G, Theruru K. Oral manifestations of human immunodeficiency virus in children: An institutional study at highly active antiretroviral therapy centre in India. J Oral Maxillofac Pathol 2012; 16(2):195-202.
  • 13
    Vaseliu N, Carter AB, Kline NE, Kozinetz C, Cron SG, Matusa R, Kline MW. Longitudinal Study of the Prevalence and Prognostic Implications of Oral Manifestations in Romanian Children Infected with Human Immunodeficiency Virus Type 1. Pediatr Infect Dis J 2005; 24(12):1067-1071.
  • 14
    Ranganathan K, Geethalakshmi E, Krishna Mohan Rao U, Vidya KM, Kumarasamy N, Solomon S. Orofacial and systemic manifestations in 212 paediatric HIV patients from Chennai, South India. Int J Paediatr Dent 2010; 20(4):276-282.
  • 15
    Miziara, ID, Weber R. Oral lesions as predictors of highly active antiretroviral therapy failure in Brazilian HIV infected children. J Oral Pathol Med 2008; 37(2):99-106.
  • 16
    Sowole CA, Orenuga OO, Naidoo S. Access to oral health care and treatment needs of HIV positive paediatric patients. Pesq Bras Odontoped Clin Integr 2009; 9(2):141-146.
  • 17
    Kumar RK, Mohan G, Reddy NV, Rao VA, Shameer M, Christopher A. Associated oral lesions in human immunodefeciency virus infected children of age 1 to 14 years in antiretroviral therapy centers in Tamil Nadu. Contemp Clin Dent 2013; 4(4):467-471.
  • 18
    Gaitán-Cepeda LA, Domínguez-Sánchez A, Pavía-Ruz N, Muñoz-Hernández R., Verdugo-Díaz R, Valles-Medina AM, Meráz-Acosta H. Oral lesions in HIV+/AIDS adolescents perinatally infected undergoing HAART. Med Oral Patol Oral Cir Bucal 2010; 15(4):e545-e550.
  • 19
    Meless D, Ba B, Faye M, Diby JS, N'zoré S, Datté S, Diecket L, N'Diaye C, Aka EA, Kouakou K, Ba A, Ekouévi DK, Dabis F, Shiboski C, Arrivé E. Oral lesions among HIV-infected children on antiretroviral treatment in West Africa. Trop Med Int Health 2014; 19(3):246-255.

Publication Dates

  • Publication in this collection
    Jan 2018

History

  • Received
    18 Apr 2015
  • Reviewed
    16 Dec 2015
  • Accepted
    18 Dec 2015
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