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ORIGINAL ARTICLE
Year : 2016  |  Volume : 19  |  Issue : 1  |  Page : 35-40

Comparative periodontal status of human immunodeficiency virus-positive patients and controls in a dedicated human immunodeficiency virus clinic in Nigeria


1 Department of Preventive Dentistry, Faculty of Dental Sciences, College of Medicine, University of Lagos, Idi-Araba, Lagos, Nigeria
2 Department of Preventive and Community Dentistry, Faculty of Dentistry, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Nigeria
3 Department of Haematology and Blood Transfusion, Faculty of Clinical Sciences, College of Medicine, University of Lagos, Idi-Araba, Lagos, Nigeria
4 Department of Medicine, Lagos State University College of Medicine, Ikeja Lagos, Nigeria

Date of Acceptance12-Apr-2015
Date of Web Publication12-Jan-2016

Correspondence Address:
K A Umeizudike
Department of Preventive Dentistry, Faculty of Dental Sciences, College of Medicine of the University of Lagos, P. M. B. 12003, Idi-Araba, Lagos
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1119-3077.164330

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   Abstract 

Background: There are diverse reports on the prevalence and severity of chronic periodontitis in human immunodeficiency virus (HIV) positive persons. Few studies have been carried out in developing countries in Sub-Saharan Africa. This study was aimed at comparing the prevalence and severity of chronic periodontitis of HIV-seropositive patients with that of HIV-seronegative persons using the community periodontal index (CPI).
Methodology: This was a comparative study of the periodontal status of 110 HIV-positive subjects and 110 age and gender-matched HIV-negative controls attending a dedicated HIV Clinic in a Teaching Hospital in Lagos, Nigeria. The CPI and simplified oral hygiene index score were used in the periodontal examination. Highest CPI scores and percentages of CPI sextants assessed the prevalence and severity of chronic periodontitis respectively. Logistic regression was used in adjusting demographic differences in the study population. P ≤ 0.05 was considered as significant.
Results: A significant proportion of the HIV-positive patients 61 (55.5%) and the HIV-negative controls 53 (48.7%) had shallow pockets (4–5 mm) (CPI code 3). The prevalence of deep pockets (≥ 6mm) (CPI code 4) was higher among HIV-positive patients 9 (8.2%) than the controls 4 (3.5%) (P = 0.079). HIV-positive patients had a greater percentage of CPI codes 3, 4 and fewer CPI code 0 sextants than controls (P = 0.000). Both groups had comparable oral hygiene status (P = 0.209). Using a logistic regression analysis, HIV-positive status and lower education accounted for the greater severity of chronic periodontitis.
Conclusion: HIV-seropositive patients had more severe chronic periodontitis than the HIV-seronegative controls, which was independent of lower education.

Keywords: Chronic periodontitis, community periodontal index, human immunodeficiency virus -positive, Nigeria


How to cite this article:
Umeizudike K A, Ayanbadejo P O, Savage K O, Nwhator S O, Akanmu A S, Ogunleye O. Comparative periodontal status of human immunodeficiency virus-positive patients and controls in a dedicated human immunodeficiency virus clinic in Nigeria. Niger J Clin Pract 2016;19:35-40

How to cite this URL:
Umeizudike K A, Ayanbadejo P O, Savage K O, Nwhator S O, Akanmu A S, Ogunleye O. Comparative periodontal status of human immunodeficiency virus-positive patients and controls in a dedicated human immunodeficiency virus clinic in Nigeria. Niger J Clin Pract [serial online] 2016 [cited 2020 Jan 23];19:35-40. Available from: http://www.njcponline.com/text.asp?2016/19/1/35/164330


   Introduction Top


Exacerbated chronic periodontitis is part of the spectrum of periodontal diseases that has been described in association with the human immunodeficiency virus (HIV) infection. As far back as the early 1990s, studies exploring the possible influence of HIV infection on conventional chronic periodontitis reported severe gingival inflammation and attachment loss in HIV-seropositive patients [1],[2] compared with HIV-negative controls.[3] Most of these studies were cross-sectional in design, although these findings were refuted in other studies among Caucasian and African HIV-positive individuals respectively.[4],[5] In an earlier longitudinal study, no differences were found in the proportion of sites affected by attachment loss at 1 mm, 2 mm or 3 mm thresholds at either time interval between the 19 HIV positive persons and 17 HIV-negative controls.[4] The more severe and extensive periodontal attachment loss observed among the HIV-positive group at baseline compared with the HIV-negative controls was attributed to their higher prevalence of smoking and poorer oral hygiene.

More recent well-controlled studies from developed [6],[7] and developing countries [8] have equally provided conflicting results. The cross-sectional Indian study carried out among HIV-positive patients using the community periodontal index (CPI) of Treatment Needs revealed significant greater periodontal breakdown in the HIV-positive cohort than age-matched controls.[8] These observations are not surprising considering the deterioration in the immune system of the host. This is hall-marked by the gradual depletion of CD4-T-cells resulting in neutrophil hyperactivity and consequent destruction of the periodontal tissues. It has been suggested that interleukin (IL-18) is elevated in HIV-positive patients and may thus play a role in the degree of periodontitis observed in HIV-positive patients.[9]

In spite of these reports, other recent studies failed to show differences in the severity of chronic periodontitis between HIV-positive and HIV-negative individuals.[10] The variation in the prevalence of chronic periodontitis has been attributed to methodological and racial differences.[4],[11] It is interesting to note that most of these studies have been conducted in well-developed countries, with few in Sub-Saharan Africa, which bears the largest burden of the HIV infection epidemic, accounting for over 60% of those affected with HIV.[12] A South African study did not find any significant differences in clinical parameters such as bleeding on probing, pocket depth or attachment loss measurements between HIV-positive and age-matched HIV-negative controls and the low CD4 + T-cell count did not appear to be a risk factor for increased severity of chronic periodontitis among the HIV-positive subjects.[13]

It is an irony that Nigeria with the second highest number of people, an estimated 3.2 million living with HIV [12],[14] has a few published reports on the periodontal status of HIV-positive persons. Recently, a Nigerian study reported the prevalence of periodontitis as 63.3% among HIV-positive patients.[15] Whether this prevalence differs from that of the HIV-uninfected population is not known. The aim of this study was therefore to compare the periodontal status of HIV-infected patients in Nigeria with that of an HIV-negative control group using the CPI, a tool developed by the World Health Organization for its simplicity and uniformity.[16]


   Methodology Top


Ethical approval

The study was in accordance with the declaration of Helsinki and was approved by the Health Research and Ethics Committee of the Institution.

Study design

This was a comparative cross-sectional, analytical study carried out at a dedicated HIV-Outpatient clinic in Nigeria. The hospital is a major referral center for most peripheral hospitals in the Lagos Metropolis of South Western Nigeria and serves a catchment population of over 18 million people of diverse ethnicity. The HIV-Outpatient clinic is a clinic dedicated to HIV-positive patients and doubles as a voluntary counseling and testing center.

Sampling and inclusion/exclusion criteria

A convenience sample of new, consecutive, confirmed HIV-seropositive patients was used. The inclusion criteria included being 18 years of age and not yet on anti-retroviral therapy. The control group consisted of age and gender-matched HIV-negative controls attending the same clinic for voluntary counseling and testing. Exclusion criteria were diabetes mellitus, current smoking habit, pregnancy, and periodontal therapy in the preceding 6 months.

Study instrument and assessment of selected periodontal parameters

Semi-structured, self-administered questionnaires were used to obtain information on the sociodemographic characteristics of the participants. This was followed by periodontal examination of the patients while seated comfortably in an upright chair in a well illuminated room. The CPI according to the WHO criteria and the Simplified oral hygiene index were utilized in assessing the periodontal status and oral hygiene status of the participants respectively.[16],[17] A single examiner (the lead author) carried out these assessments thus eliminating inter-examiner variability. The highest CPI score was recorded for each subject and was used to determine the prevalence of chronic periodontitis. The CPI parameters included CPI score 0 representing healthy periodontal status, CPI 1 (bleeding), CPI 2 (calculus), CPI 3 (shallow pocket) and CPI 4 (deep pocket). The number and percentages of CPI sextants were used to assess the severity of chronic periodontitis. Sextant analyses were performed to overcome the limitations of CPI in assessing periodontal status. The values of the CD4 + cell counts determined at the time of periodontal examination were obtained from the patients' hospital record.

Statistical analysis

Data were analyzed using SPSS 17 (SPSS Inc. Chicago, USA) statistical software. Pearson's Chi-square tests of association, t-test and analysis of variance were used to compare qualitative and quantitative variables where appropriate. Logistic regression analysis was used to determine the association between HIV status and severity of periodontitis (CPI sextants with codes 3, 4) while adjusting for significant demographic variables in the bivariate analysis. Analyses were performed at 95% confidence level therefore P ≤ 0.05 was considered statistically significant.


   Results Top


Socio-demographics

A total of 110 HIV-positive patients and 110 HIV-negative controls were enrolled into the study. Of the HIV-positive patients, 76 (69.1%) were females and 34 (30.9%) were males, giving a female: male ratio of 2.2–1. The mean age (standard deviation) of the HIV-positive patients and HIV-negative controls were 35.4 (±10.2) years and 34.9 (±10.5) years respectively (P = 0.734). Secondary school education was the level attained by most 53 (48.2%) of the HIV-positive patients while the tertiary level of education was predominant in most 47 (42.7%) of the HIV-negative controls. The association between educational level and HIV status was significant (P = 0.001). Unskilled workers constituted the majority occupation in both HIV-positive patients 54 (49.1%) and HIV-negative subjects 35 (31.8%), as shown in [Table 1]. However, HIV-positive patients had significantly fewer professionals (10%) than the HIV-negative controls (27.3%) (P = 0.005) [Table 1].
Table 1: Baseline characteristics of study population

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Oral hygiene status

Most of the HIV-positive patients (52.7%) had a fair oral hygiene, which was comparable to that of the HIV-negative controls (52.7%). Although, more of the HIV-positive patients (16.4%) had poor oral hygiene compared to the HIV-negative controls (9.1%), the difference was not statistically significant (P = 0.209).

Prevalence of chronic periodontitis in the study population

[Figure 1] shows the prevalence of chronic periodontitis in the study population. Most (55.5%) of the HIV-positive patients had shallow pockets (CPI 3), followed by calculus (CPI 2) (33.6%). Shallow pockets were also predominant in the HIV-negative controls (48.2%), followed by Calculus in 37.3%. Although, the HIV-infected patients had a higher percentage of deep pockets (CPI 4) than the controls (8.2% vs. 3.6% respectively) the difference failed to attain statistical significance (P = 0.079).
Figure 1: Prevalence of chronic periodontitis in study population

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Severity of chronic periodontitis in the study population

The association between the severity of chronic periodontitis and HIV status was determined using bivariate analysis [Table 1]. The HIV-positive patients had a higher percentage of CPI sextants with codes 3 and 4 (19.7% and 2.1% respectively) compared to the HIV-negative controls (13.9% and 0.6% respectively). Also of note were the fewer percentages of healthy CPI sextants (code 0) in the HIV-positive patients (15.3%) than the HIV-negative controls (27.1%). These associations were statistically significant (P = 0.000). [Table 2] reveals the relationship between severity of periodontitis and CD4 + cell counts, which did not find any statistically significant association (P = 0.623). After adjusting for the effect of education and occupation in the regression model, the independent factors accounting for the greater severity of periodontitis in HIV-positive patients were HIV infection and lower level of education [Table 3].
Table 2: Association of CD4+ cell counts with severity of chronic periodontitis

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Table 3: Logistic regression of factors associated with severity of chronic periodontitis

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   Discussion Top


The present study compared the periodontal status of HIV-positive patients against HIV-negative controls in Nigeria. As far as the authors know, this is the first documented study reporting this. This study indicates that HIV-positive patients have the significantly greater severity of chronic periodontitis than age and gender matched, healthy HIV-negative controls. This was reflected by the higher number of CPI sextants with codes 3 and 4 in the HIV-positive patients (21.8%) than the HIV-negative controls (14.5%). It was further supported by the fewer CPI sextants with code 0 among the HIV-positive patients (14.3%) than in the HIV-negative controls (27.1%). This finding is in agreement with the Indian study from another developing country.[8] The Indian cross-sectional study is similar to the present study in that a comparable periodontal index was used to assess the periodontal status.[8] They reported the significantly greater number of CPITN sextants with shallow and deep pockets among HIV-positive patients than age-matched presumably HIV-negative controls with similar socio-economic status. Thus, subjects in the control group had better periodontal health compared with the HIV-positive patients. However, their presumption for the HIV-negative group could affect the reliability of their findings.

In another related study among HIV-infected persons in Poland, more advanced periodontal changes were observed in the HIV-infected subjects such that as HIV infection time increased, there was decrease of the number of healthy CPI sextants, compared to the HIV-negative subjects.[7] This may be due to the deterioration in their immune system, characterized by a gradual depletion of the CD4 lymphocytes, which compromises the dento-gingival region. Higher levels of potent pro-inflammatory cytokines such as IL-8 have been described in HIV infection and believed to contribute to the etiopathogenesis of periodontitis observed in HIV-positive patients.[9]

Overall, the prevalence of combined shallow and deep pockets (CPI codes 3, 4) in the present study was 63.7%. This was much higher than that of the HIV-negative controls (51.7%). The higher prevalence figures observed in the present study may be attributable to the poor dental visiting behavior observed among Nigerians generally.[18],[19] These values are considerably high for persons in age groups below 45 years, but are still much lower than the Indian study, which was 78.3% and 58.6% in HIV-positive and presumably HIV-negative respectively.[8] The generally low socioeconomic status of the Indian subjects could have accounted for this observation. Our findings contrast against a previous study in Tanzanian, which failed to detect any significant difference in bleeding on probing, pocket depth and attachment loss between HIV-seropositive and HIV-seronegative controls.[5] The current study however, excluded some important confounders for chronic periodontitis such as smoking and diabetes which have been identified as important risk factors in the prevalence and severity of periodontitis. The present study highlighted the effect of lower education on the severity of periodontitis, which has been documented in literature.[20] HIV-positive status remained an independent risk factor to the severity of periodontitis in this cohort. The present study was cross-sectional by design and may be limited in actually proving a causal relationship between HIV infection and severity of periodontitis. It has however provided baseline data upon which future longitudinal studies can be conducted. It is noteworthy that there may be difficulties in conducting studies on the natural association between HIV infection and chronic periodontitis for ethical reasons.

Significant education and occupation-related differences were noticed between the HIV-positive and HIV-negative groups in the present study. In spite of these observations, few well controlled studies [5],[13],[21] exist on the prevalence and severity of chronic periodontitis in sub-Saharan Africa. The fact that the patients seen in the present study were recruited from outpatient medical clinics, instead of the dental clinics could also explain the lower prevalence of chronic periodontitis in the study. The patients in this study were also mostly seen immediately after HIV diagnosis, at the early stage of the infection, thus implying a lesser time for more severe chronic periodontitis to develop.

Furthermore, higher mean CD4+ cell counts ≥ 200 cells/mm 3 may explain the low prevalence of deep pockets (CPI code 4), which is more common among persons with immunosuppression as corroborated by a Finnish report.[6] The higher prevalence and severity of chronic periodontitis observed among the HIV-positive patients than the HIV-negative subjects in this study underscores the importance of early diagnosis and treatment of chronic periodontitis, which can be achieved through regular maintenance dental recalls. Although, findings from a recent South-African study did not support our observation, the difference may be attributed to the fact that the control group in their study comprised subjects with unconfirmed, presumably HIV-sero-negative.[13] Some of the controls could have been HIV seropositive, which may have affected the outcome of their findings. Another possible reason for the disparity may be connected with the difference in the criteria used to define chronic periodontitis in their study as they utilized periodontal probing depths and gingival marginal recession.[13] However, the smaller sample size in their study may have also affected the outcome since a larger sample size was evaluated in the present study.

Although HIV-positive patients had poorer oral hygiene status than controls in the present study, the difference was not statistically significant. Hence, the poorer oral hygiene is unlikely to influence affect the greater severity of periodontitis observed among the HIV-positive patients. Moreover, it has been suggested the relationship of oral hygiene to periodontitis is less straightforward and may not affect the host response.[22] Unfortunately, few studies are available in the literature to compare and validate these findings. No doubt, there is an urgent need for well-designed longitudinal studies to clarify the grey areas between the periodontal status of HIV-positive and HIV-negative persons.


   Conclusions Top


Human immunodeficiency virus -positive patients in this study had significantly poorer periodontal status than HIV-negative controls, which was attributed to their HIV infection and lower level of education.

This highlights the need for regular periodontal screening of HIV-positive patients and early treatment of diagnosed periodontitis while working in collaboration with HIV specialists to improve the overall quality of life of the patients.


   Acknowledgment Top


The authors would like to thank the staff of the AIDS Prevention Initiative Nigeria (APIN) at the Lagos University Teaching Hospital for their assistance during the study.

 
   References Top

1.
Friedman RB, Gunsolley J, Gentry A, Dinius A, Kaplowitz L, Settle J. Periodontal status of HIV-seropositive and AIDS patients. J Periodontol 1991;62:623-7.  Back to cited text no. 1
    
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Barr C, Lopez MR, Rua-Dobles A. Periodontal changes by HIV serostatus in a cohort of homosexual and bisexual men. J Clin Periodontol 1992;19:794-801.  Back to cited text no. 2
    
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Robinson PG, Sheiham A, Challacombe SJ, Zakrzewska JM. The periodontal health of homosexual men with HIV infection: A controlled study. Oral Dis 1996;2:45-52.  Back to cited text no. 3
    
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Robinson PG, Boulter A, Birnbaum W, Johnson NW. A controlled study of relative periodontal attachment loss in people with HIV infection. J Clin Periodontol 2000;27:273-6.  Back to cited text no. 4
    
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Scheutz F, Matee MI, Andsager L, Holm AM, Moshi J, Kagoma C, et al. Is there an association between periodontal condition and HIV infection? J Clin Periodontol 1997;24:580-7.  Back to cited text no. 5
    
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Mellanen L. The Influence of HIV Infection to the Periodontium; a Clinical, Microbiological, and Enzymological Study. Doctorate Dissertation; 2006 Available from: http://www.ethesis.helsinki.fi/julkaisut/laa/hamma/vk/mellanen/. [Last accessed on 2014 Dec 04].  Back to cited text no. 6
    
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Choromanska M, Waszkiel D. Periodontal status and treatment needs in HIV-infected patients. Adv Med Sci 2006;51 Suppl 1:110-3.  Back to cited text no. 7
    
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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;18:55-9.  Back to cited text no. 8
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Falasca K, Vecchiet F, Ucciferri C, Vignale F, Conti P, Pizzigallo A, et al. Periodontitis and cytokine patterns in HIV positive patients. Eur J Med Res 2008;13:163-8.  Back to cited text no. 9
    
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Fricke U, Geurtsen W, Staufenbiel I, Rahman A. Periodontal status of HIV-infected patients undergoing antiretroviral therapy compared to HIV-therapy naive patients: A case control study. Eur J Med Res 2012;17:2.  Back to cited text no. 10
    
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Barr CE. Periodontal problems related to HIV-1 infection. Adv Dent Res 1995;9:147-51.  Back to cited text no. 11
    
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UNAIDS AIDS Info; 2014 Epidemiological Status. Available from: http://www.unaids.org/en/dataanalysis/datatools/aidsinfo. [Last accessed on 2014 Nov 16].  Back to cited text no. 12
    
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Khammissa R, Feller L, Altini M, Fatti P, Lemmer J. A Comparison of chronic periodontitis in HIV-seropositive subjects and the general population in the Ga-Rankuwa Area, South Africa. AIDS Res Treat 2012;2012:620962.  Back to cited text no. 13
    
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Federal Republic of Nigeria Global Aids Response Country Progress Report Nigeria; 2014. Available from: http://www.unaids.org/sites/default/files/country/documents/NGA_narrative_report_2014.pdf. [Last accessed on 2014 Nov 16].  Back to cited text no. 14
    
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Umeizudike KA, Ayanbadejo PO, Savage KO, Akanmu AS, Nwhator SO, Emeka C. Prevalence and Determinants of Chronic periodontitis in HIV positive patients in Nigeria. Asian Pac J Trop Dis 2014;4:306-12.  Back to cited text no. 15
    
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18.
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19.
Umeizudike KA, Ayanbadejo PO, Taiwo OA, Savage KO, Alade GO. Utilization of dental services by administrative workers in a Tertiary Health Institution in Lagos, Nigeria – A pilot study. Niger Q J Hosp Med 2014;24:86-90.  Back to cited text no. 19
    
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21.
Ndiaye CF, Critchlow CW, Leggott PJ, Kiviat NB, Ndoye I, Robertson PB, et al. Periodontal status of HIV-1 and HIV-2 seropositive and HIV seronegative female commercial sex workers in Senegal. J Periodontol 1997;68:827-31.  Back to cited text no. 21
    
22.
Burt B, Research, Science and Therapy Committee of the American Academy of Periodontology. Position paper: Epidemiology of periodontal diseases. J Periodontol 2005;76:1406-19.  Back to cited text no. 22
    


    Figures

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    Tables

  [Table 1], [Table 2], [Table 3]


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