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Table of Contents   
ORIGINAL RESEARCH  
Year : 2011  |  Volume : 22  |  Issue : 5  |  Page : 732
Comparison of oral manifestations with CD4 count in HIV-infected patients


1 Department of Oral Medicine and Radiology, Nair Hospital Dental College, Mumbai, India
2 Department of Oral Medicine and Radiology, Government Dental College and Hospital, Mumbai, India

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Date of Submission27-Jul-2010
Date of Decision07-Apr-2011
Date of Acceptance09-Aug-2011
Date of Web Publication7-Mar-2012
 

   Abstract 

Aim and Objective: This study was carried out with the primary aim of correlating oral changes and general changes of HIV-infected patients with their CD4 count.
Materials and Methods: 124 patients were selected, and after taking their informed consent, they were subjected to detailed history taking and thorough clinical examination. Specific oral lesions and general physical changes were recorded. Every patient was subjected to laboratory investigation for CD4 count. All these findings were tabulated. The clinical observation and laboratory findings were subjected to critical analysis and correlated. Statistical test, i.e. Student's " t" test, was applied and objective conclusions were drawn.
Result: Out of 124 patients, 40 had oral candidiasis, 6 had oral hairy leukoplakia, 12 had periodontal disease, 20 had xerostomia, 30 had melanin pigmentation, while 4 had HSV2, and atypical ulceration. Out of 40 patients with oral candidiasis, 28 patients had CD4 count <200 (group A), 10 patients were in group, B (CD4 count 200-500 cell/mm 3 ) and 2 patients in group C(CD4 >500 cell/mm 3 ). Oral hairy leukoplakia occurred in equal proportions in group A and B. These periodontal diseases were more commonly in group B; xerostomia and melanin pigmentation was equally seen in group A and B.
Conclusion: Oral candidiasis, oral hairy leukoplakia, linear gingival erythema, necrotizing ulcerative gingivitis, and necrotizing ulcerative periodontitis are specific oral indicators which will definitely suggest to the dental surgeon that the disease is running a rapid downhill course and due to this the oral physician is in a position to raise a suspicion and alert the general physician regarding the declining immune status of patient.

Keywords: CD4 count, cluster of differentiation, seropositive

How to cite this article:
Sontakke SA, Umarji H R, Karjodkar F. Comparison of oral manifestations with CD4 count in HIV-infected patients. Indian J Dent Res 2011;22:732

How to cite this URL:
Sontakke SA, Umarji H R, Karjodkar F. Comparison of oral manifestations with CD4 count in HIV-infected patients. Indian J Dent Res [serial online] 2011 [cited 2019 Aug 18];22:732. Available from: http://www.ijdr.in/text.asp?2011/22/5/732/93470
The Human Immunodeficiency Virus (HIV)/AIDS global epidemic has greatly exceeded earlier predictions and it is now clear that it has the potential to affect all countries and population groups. The number of people infected with the HIV continues to increase rapidly. India, with its unique demographics, has the dubious distinction of having the largest number of the people living with HIV outside of South Africa. [1]

A wide body of scientific research attests to the frequency of oral disease in persons living with HIV disease and AIDS. Oral lesions are often clearly visible and several can be diagnosed accurately by clinical features alone. The mouth and pharynx are easily examined by clinicians with a wide range of professional training.

Till date, CD4 cell count and viral load are recognized and widely used as markers of HIV-related disease progression. However, laboratory parameters will only partially reflect disease stage and progression, the additional clinical marker will more accurately represent the patient's overall disease status. [2] Considering the individual significance of CD4 cell count and oral lesions in assessing the disease status, it was thought worthwhile to correlate the two parameters, viz. CD4 cell count and oral lesions, in HIV/AIDS patients. This study was undertaken to assess the efficacy of oral changes as an indicator of disease status in HIV/AIDS.

Aims and objectives

The basic aims and objective of this study were i) to diagnose and record the oral changes in patients who were seropositive and having full-blown AIDS; ii) to determine CD4 count of all the above patients; and iii) to correlate between presence/absence and severity of oral changes and individual CD4 count.


   Materials and Methods Top


The patients attending the AIDS Research and Control Center (ARCON) at the JJ group of Hospital, Byculla, and OPD of Bell Air Hospital, who had positive laboratory findings, were selected for the study. The patients attending the Government Dental College and Hospital OPD with suspicious lesions were advised laboratory tests, and if found to be seropositive, they were included in this study. In general, all the seropositive patients with or without oral changes were included in the study. The patients on antiretroviral therapy (ART) were also included. Each patient selected for this study was subjected to a detailed case history and laboratory investigation for CD4 cell count. Prior consent was taken from every selected patient. The result was statistically evaluated by Student's "t" test and analyzed.


   Results and Discussion Top


The oral lesions like candidiasis, linear gingival erythema (LGE), necrotizing ulcerative gingivitis (NUG), etc. were then categorized according to the specific group. In this study of 124 patients, the mean CD4 count was 277 cells/mm 3 . The CD4 count ranged from 3 to 990 cells/mm 3 . The normal CD4 count ranges between 430 and 1300 cells/mm 3 , but it is generally above 800 cells/mm 3 in healthy persons. The mean age of patient in this study was 33 years (ranging from 7 to 62 years). Among the 124 patients, there was definitely male preponderance with 80 males and 44 females. All adults included in this study were heterosexual (123 patients), and there was a solitary case of 7-year-old child who reported with vertical transmission, with the history of mother being HIV positive.

All the patients were subjected to CD4 count, and for the purpose of comparison, three groups were formed:

group A: <200 CD4 cells/mm 3 and <14%;

group B: 200-500 CD4 cells/mm 3 and 14-28%; and

group C: >500 CD4 cells/mm 3 and >29%.

[Table 1] shows the distribution of oral lesions in 124 HIV and AIDS patients included in the study. In this study, the most common oral lesion was oral candidiasis. It was observed in 40 of 124 patients (32.25%). Similar findings have been observed by Palmer, [3] Anil, [4] Nittyanannta, [5] Kerdpon, [6] Lim, [7] Schulten, [8] and Lauren. [9] Of the candidiasis cases [Figure 1] and [Figure 2] observed in this study, pseudomembranous candidiasis was the most common variant [25 of 40 patients (20.1%)] [Table 1]. These findings are similar to those observed by Anil [4] and Nittyananttan. [5] Arendorf [10] and Palmer, [3] however, showed erythematous candidiasis to be more common than pseudomembranous candidiasis. The occurrence of pseudomembranous candidiasis in this study was low compared to the findings of other studies (13.5-66%) by Anil [4] and Nittyanantta, [5] but high compared to the findings of Arendorf [10] and Palmer. [3] Erythematous candidiasis was found in 10 cases (8.06%) compared to other studies where it ranged from 3.8 to 23.5%. Angular cheilitis in this study was found in 12.5% of cases, whereas in other studies it was 5.9-13.8% as reported by Palmer, [3] Nittayananta, [5] Arendorf, [10] Kerdpon, [6] Schulten, [8] Margiotta, [11] and Moniaci. [12]
Table 1: Distribution of oral lesion in this study and percentage given in brackets

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Figure 1: Oral candidiasis (pseudomembranous type)

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Figure 2: Culture of Candida

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We found a close association between the patient's immune status and the presence of oral candidiasis. With an increase in frequency of oral candidiasis, CD4 lymphocyte count decreased. Forty patients in this study presented with oral candidiasis; out of these, 28 patients had CD4 count < 200 cells/mm 3 (group A), 10 patients were in group B (CD4 count 200-500 cells/mm 3 ), and 2 cases were in group C. Out of 25 cases of pseudomembranous candidiasis, 19 were having CD4 count within the range of group A, five patients were in group B (200-500 cells/mm 3 CD4 cell count) and one was in group C (>500 cells/mm 3 CD4 cell count). Phelan et al., [13] found that a CD4 count less than 200 cells/mm 3 or the presence of oral candidiasis at the time of data collection increased the risk of death or development of AIDS and such prognosis was worse if both the factors were present at the onset of evaluation. This relation between oral candidiasis and low CD4 lymphocyte counts allowed us to interpret that the presence of oral candidiasis is an indirect marker of immune status of an HIV-infected patient when a CD4 count is unavailable. Adurongbanga, [14] Hodgson, [15] and Schmidt [16] showed similar findings, with most candidiasis occurring when the CD4 count was less than 200 CD4 cells/mm 3 .

Erythematous candidiasis and angular chelitis also occurred commonly in group A, i.e. 5 cases and 10 cases, respectively. The occurrence of erythematous candidiasis and angular cheilitis was less common in group B and group C. Similar findings were reported by Adurongbanga, [14] Hodgson [15] and Eyeson. [17]

Periodontal disease manifestation in HIV-infected individuals includes LGE, NUG, and necrotizing ulcerative periodontitis (NUP) [Figure 3]. Periodontal disease in this study was seen in 12 patients (9.6%). Of these, LGE was recorded in 3 patients (2.4%), NUG in 2 cases (1.61%) and NUP was seen in 7 cases (5.46%) [Table 1]. NUP was the most common of all periodontal diseases. The periodontal disease in other studies by Anil, [4] Nittyanantta, [5] Lim, [7] Schulten [8] and Margiotta [11] was reported to be in the range from 2.9 to 16%.
Figure 3: Necrotizing ulcerative periodontitis (NUP)

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The periodontal disease occurred in less severe immunosuppression, with its mean CD4 count being 290 cells/mm 3 . These periodontal diseases were more common in group B (200-500 CD4 cells/mm 3 ). Three patients had LGE with CD4 count within the range of group B. No case of LGE was found in group A and group C. Two patients who had NUG were with CD4 count between 200 and 500 cells/mm 3 (group B), with none in group A and group C [Table 1]. NUP was the most common periodontal disease that occurred in group A and group B, with no difference. No case of NUP was found in group C.

Oral hairy leukoplakia [Figure 4] was reported in 6 patients (4.13%). This was much less compared to the numbers reported by Palmer, [3] Anil, [4] Nittyannantta, [5] Arendorf, [10] Kerendpon, [6] Schultem, [8] Lauren [9] and Marigiotta. [11] The findings reported by Lim [7] were similar to ours.
Figure 4: Hairy leukoplakia

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Oral hairy leukoplakia occurred in equal proportion in groups A and B and none occurred in group C. We found that hairy leukoplakia was not associated with increasing level of immunosuppression because the presence of this oral lesion did not significantly increase as the CD4 cell count decreased. These findings are consistent with the findings of studies carried out by Hodgson, [15] Schimidt, [16] and Eyeson. [17] Very few cases of hairy leukoplakia have been reported with CD4 count >500 cells/mm 3 . Depletion of CD4 cells, as seen in progressive HIV-related disease, has been shown to accompany activity of Epstein-Barr virus (EBV) infection.

Xerostomia was found in 20 patients out of 124 (16.12%) in this study. The occurrence rate was much higher in this study compared to other studies where it ranged between 7 and 63%, as reported by Nittyanantta [5] and Laskaris. [18] Palmer [3] found that 2% of 456 patients had xerostomia.

Several medications used in the treatment of HIV-related disease may cause xerostomia. Similarly, many HIV-infected patients are prescribed tricyclic antidepressants that are associated with reduced salivary flow. It was not possible to determine if the observed xerostomia was directly related, HIV related disease or a result of medications. Our finding of xerostomia in groups A and B was nearly the same [9 cases (7.22%) and 8 (6.45%) cases, respectively]. Only 3 (2.4%) cases were reported in group C.

Reduction of salivary flow may occur as a result of HIV infection, as a side effect of anti-HIV medication or in association with significant major salivary disease. It has been found that specific salivary gland diseases, such as Sjogren's like syndrome, diffuse CD8 lymphocytic infiltration and lymphoepithelial cyst, occur during the course of HIV disease progression. The mechanism of salivary gland disease is not well understood. Several factors have been suggested to be responsible, including viral infections of the salivary gland tissues with HIV, cytomegalovirus, or EBV. [19]

Atypical ulceration, including recurrent aphthous ulcer, is occasionally found in HIV-infected patients. In this study, the lesions were diagnosed in 4 patients (3.2%), whereas other studies showed occurrence of atypical ulceration including recurrent aphthous ulcer [Figure 5] within 3-13%, as reported by Anil, [3] Nittyanantta, [19] Arendorf, [10] Kerdpon, [6] Lim, [7] Lauren, [9] Margiotta, [11] and Moniaci. [12]
Figure 5: Aphthous ulceration

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Atypical ulceration occurred more commonly in less severe immunosuppression, i.e. 2 cases (1.6%) in group B (200-500 cells/mm 3 CD4 cell count) and 1 case each in group A (<200 cells/mm 3 CD4 count) and group C (>500 cells/mm 3 CD4 cell count). The findings of this study are similar to those of Eyeson. [17]

Herpes simplex virus (HSV) infection was found in 1.81%. This finding is similar to the findings of Palmer. [4] Nittyanantta, [19] Arendorf [10] and Kerdpon [6] reported an incidence ranging from 0.41 to 4.8%.

HSV infection occurred in two patients and both were having CD4 count below 200 cells/mm 3 (group A). These findings on HSV infection are similar to that reported by Adurongbanga. [14]

Melanotic pigmentation was found in 38 patients (30.6%). In other studies, it was reported to range from 0.4 to 6.7%. HIV-seropositive patients with opportunistic infections may have adrenocortical involvement by a variety of parasites, which manifests the signs and symptoms of Addison's disease. Such patients undergo progressive hyperpigmentation of the skin, nails, and mucus membranes. In actuality, most HIV-seropositive patients presenting with diffuse multifocal macular brown pigmentations of the buccal mucosa show no features of adrenocortical disease. The oral pigmentation cannot be attributed to medications in this population because cases have been recorded in individuals who have not received any medications that could be so implicated. Thus, the etiology remains undetermined. [20]

Melanin pigmentation occurred commonly in group A (<200 cells/mm 3 CD4 cell count) and group B (200-500 cells/mm 3 CD4 cell count) with CD4 count less than 500 cells/mm 3 . The mean CD4 count of this oral lesion is 270 cells/mm 3 . Melanin pigmentation in HIV infection may be because of infection of the adrenal gland. With the increase in immunosuppression, there are greater chances of adrenocortical involvement by a variety of parasites giving rise to adrenal insufficiency and signs and symptoms similar to Addison disease. [20] Drugs like azidothymidine used in ART have also been associated with pigmentation.

Loss of taste sensation was noted in 2.41% of patients.


   Conclusions Top


  • Out of 124 HIV patients, 88 showed oral changes. Candidiasis was the most common oral lesion (P<0.05).
  • Average CD4 count was found to be 277 cells/mm 3 . The distribution of patients was 49 in group A (with CD4 count <200 cells/mm 3 ), 60 patients in group B (with CD4 count 200-500 cells/mm 3 ) and 15 patients in group C (with CD4 count >500 cells/mm 3 ).
  • The frequency of oral lesion was seen to be maximum in group A and group B, i.e. CD4 count <500 cells/mm 3 , and candidiasis was found to be more common in group A (with CD4 count <200 cells/mm 3 ). Pseudomembranous candidiasis was more common than erythematous candidiasis and angular cheilitis in group A.


It must be understood and appreciated that various pathological changes manifested generally in the oral cavity will have multifactorial etiology, viz. patients being in immunocompromised state, change in the bacterial flora, other factors which facilitate infections by different organisms and trigger off unusual neoplastic lesions, etc.

Even if definite conclusion can be drawn about a positive correlation between oral lesions and CD4 count, it is worthwhile mentioning that oral candidiasis, oral hairy leukoplakia, LGE, NUG and NUP are specific oral indicators which will definitely suggest to the dental surgeon that the disease is running a rapid downhill course, and due to this, the oral physician is in a position to raise a suspicion and alert the general physician regarding the declining immune status of the patient.

 
   References Top

1.Clinical Management of HIV and AIDS at District Level. New Delhi: WHO regional office South East Asia; 1998.  Back to cited text no. 1
    
2.Michel Glick BC. Oral manifestation associated with HIV related disease as a marker for immune suppression and AIDS. Oral Surg Oral Med Oral Pathol 1994;77:344-9.  Back to cited text no. 2
    
3.Plamer GD. Aetiology of oral manifestation of oral manifestation of HIV. Oral Dis 1996;2:193-7.  Back to cited text no. 3
    
4.Anil S, Challacombe SJ. Oral lesion of HIV and AIDS in Asia: An overview. Oral Dis 1997;3(suppl 1): S36-4.  Back to cited text no. 4
    
5.Chungpanich NS. Oral lesion in group of Thai people with AIDS. Oral Dis 1997;3(suppl 1): S41-5.  Back to cited text no. 5
    
6.Kerdpon D, Pongsiriwet S, Pangsomboon K, Iamaroon A, Kampoo K, Sretrirutchai S, et al. Oral manifestations of HIV infection in relation to clinical and CD4 immunological status in northern and southern Thai patients. Oral Dis 2004;10:138-44.  Back to cited text no. 6
    
7.Lim Ysllnr AA. Oral manifestations of human immunodeficiency virus (HIV)-infected patients in Singapore. Ann Acad Med Singapore 2001;30:600-6.  Back to cited text no. 7
    
8.Shulten EA. Oral manifestation of HIV infection in 75 Dutch patient. J Oral Pathol Med 1989;18:42-6.  Back to cited text no. 8
    
9.Patton LL, McKaig R, Strauss R, Rogers D, Eron JJ Jr. Changing prevalence of oral manifestations of human immuno-deficiency virus in the era of protease inhibitor therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;89:299-304.  Back to cited text no. 9
    
10.Arendorf TM, Bredekamp B, Cloete C, Wood R, O'Keefe E. Intergroup comparison of HIV oral candidiasis in South Africans. Oral Dis 1997;3 (suppl 1): S54-7.  Back to cited text no. 10
    
11.Margiotta V. HIV infection: Oral lesions, CD+ cell count and viral load in an Italian study population. J Oral Pathol Med 1999;28:173-7.  Back to cited text no. 11
    
12.Moniaci D, Greco D, Flecchia G, Raiteri R, Sinicco A. Epidemiology clinical features and prognostic value of HIV 1 related oral lesion. J Oral Pathol Med 1990;19:477-81.  Back to cited text no. 12
    
13.Phelan JA, Klein RS. Resolution of hairy leukoplakia during treatment with Azidothymidine. Oral Surg Oral Med Oral Pathol 1988;65:717-20.  Back to cited text no. 13
    
14.Adurongbanga MI. Orofacial lesions in HIV/AIDS adults in Nigeria. Oral Dis 2004;10:319-26.  Back to cited text no. 14
    
15.Hodgson T. HIV associated oral lesion: Prevalence in Zambia. Oral Dis 1997;3(suppl 1): S46-50.  Back to cited text no. 15
    
16.Schimidt-Westhausen A. Oral manifestation in 70 German HIV infected women. Oral Dis 1997;3(suppl 1): S28-30.  Back to cited text no. 16
    
17.Eyeson JD, Tenant-Flowers M, Cooper DJ, Johnson NW, Warnakulasuriya KA. Oral manifestation of HIV positive cohort in the era of highly active antiretroviral therapy (HAART) in South London. J Oral Pathol Med 2002;31:169-74.  Back to cited text no. 17
    
18.Laskaris G, Potouridou I, Laskaris M, Stratigos J. Gingival lesions of HIV infection in 178 Greek patients. Oral Surg Oral Med Oral Pathol 1992;74:168-71.  Back to cited text no. 18
    
19.Nittayananta W, Chungpanich S. Oral lesion in group of Thai people with AIDS. Oral Dis 1997;3(suppl 1): S41-5.  Back to cited text no. 19
    
20.Burkit's. Oral Medicine Diagnosis and treatment, infectious diseases. 10 th ed. New Delhi, India: BC Decker Inc, Elsevier; 2003. p. 542.  Back to cited text no. 20
    

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Correspondence Address:
Subodh Arun Sontakke
Department of Oral Medicine and Radiology, Nair Hospital Dental College, Mumbai
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0970-9290.93470

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    Figures

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