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On-line version ISSN 1806-4841
An. Bras. Dermatol. vol.78 no.1 Rio de Janeiro Jan./Feb. 2003
CLINICAL, LABORATORY AND THERAPEUTIC INVESTIGATION
Epidemiologic profile of HIV - positive patients with dermatoses in Natal/RN /Brazil*
Fernando CardosoI; Heloísa RamosII; Márcio LoboIII
IMaster Degree, "Universidade Federal
de Pernambuco". Dermatologist, "Universidade de São Paulo-Ribeirão Preto". Head
of Teaching Dept., Sanitary Dermatology, "Hospital de Infectologia Giselda Trigueiro",
Natal/Rio Grande do Norte State
IIMaster Degree, "Universidade de São Paulo". PhD, "Universidade de São Paulo". Adjunct-Professor, "Universidade Federal de Pernambuco". Head of the Infirmary of the Medical Clinic at the "Hospital das Clínicas"
IIILecturer, "Universidade Federal de Pernambuco". Titular Professor of Dermatology, Tropical Medicine Department of the "Universidade Federal de Pernambuco". Coordinator of Post-graduate Studies in Tropical Medicine at the "Universidade Federal de Pernambuco"
There is no description of dermatoses among HIV infected individuals in Rio
Grande do Norte(RN) / Brazil, althoug this state had an accumulated total of
899 adult Aids cases registered from january 1983 to august 2000 and mortality
coefficients per 100,000 residents of 3.80 and 2.47, in the years 1995 and 1997,
respectively, such that this difference in values coincided with the introduction
of antiretroviral (ARV) usage in this state.
OBJECTIVE: To describe epidemiologic caracteristics of retrovirus infected subjects with dermatoses, including frequency of dermatoses and to establish relationships between the caracteristics of users and nonusers of ARV drugs.
MATERIAL AND METHODS: Were included 172 patients, according to HIV infection classification of CDC/1992. The use of ARV drugs was determined and the dermatoses were submited to analysis.
RESULTS: The sample comprises 83.72% of men, with mean age of 37.17 years, with sexual way of retrovirus contamination (96.5%), predominant heterossexual behaviour (54.7%). The most frequent form skin diseases were classified into viral, fungic and miscellaneous. The mean percentage of diseased skin area was 12.5%. Mean viral load was 109,114.05 cps/ml, and mean CD4+ T lymphocytes was 383.15 cells/mm3. Overal 81.4% of patients were using ARV drugs.
CONCLUSIONS: The epidemiologic profile of HIV infected patients residents in state of RN did not differ from that of others brazilian regions. Analytic studies, minimizing confounding bias, are necessary to discribe the real frequency of HAART (High Active Antiretroviral Therapy) in seropositive HIV subjects.
Keywords: skin diseases; epidemiology; acquired immunodeficiency syndrome
According to data from the National Coordination of Sexually Transmissible Diseases and Aids of the Ministry of Health, since the beginning of the epidemic up until 06/03/2000, 190,949 cases of Aids have been notified in Brazil. Most cases are concentrated in the Southeast area with an accumulated incidence coefficient of 210 up to June 03, 2000; the remaining areas present the following coefficients: South (131); Central-west (102.1); Northeast (40.9) and North (36.4).
The number of cases of Aids in adults in Rio Grande do Norte, presented in the Notification System (Sinan) of the State General Office of Health of Rio Grande do Norte, from January 1983 to August 26, 2000 was 899, of which 675 were male and 800 in the 20 to 49-year-old age group.
Natal and Mossoró, reference centers for infectious diseases in the state, contributed with 596 and 59 notifications, respectively.
Regarding the diseases associated to retrovirus, a great frequency of dermatoses were observed with etiologies including infectious and parasitic; neoplastic; and inflammatory, auto-immune or multifactorial.1-8
The CD4+ helper cells count in the peripheral blood is a laboratorial marker of the progression of immunodeficiency induced by HIV, and the number of copies of viral RNA is a predictor of the degree of immunodeficiency, irrespective of the CD4+ T lymphocyte counts.7,14-16
The use of highly effective antiretroviral medicines (or Highly Active Antiretroviral Therapy - HAART) since 1995, has triggered changes in the presentation and course of the dermatoses in those infected by a retrovirus and can promote the disappearance of cutaneous lesions and prevent more serious opportunist diseases, following a partial recovery of the immunological system.17
The present study was performed at the Hospital Giselda Trigueiro, in Natal/RN, a reference center for infectious and contagious diseases in the capital and that registered 66.3% of the Aids notifications in the state from January 1983 to August 2000.
This work enabled a documentation of the epidemic and immunological characteristics of a sample infected by HIV, the frequency of dermatoses and their relationship in terms of: the percentage of body surface involved, the CD4+ T lymphocyte count and viral load, as well as the use of antiretroviral medicines.
PATIENTS AND METHODS
The Commission of Medical Ethics of the Hospital Giselda Trigueiro (HGT) in Natal/RN approved the study. Informed and written consent was obtained from all participants.
A total of 381 patients over 13 years of age and infected by HIV were evaluated according to the presence of dermatoses. The patients were interviewed when they sought a specialized Aids clinic and were hospitalized, for operational reasons, in the first five equal-numbered beds of the Aids infirmary during the period from September 01, 1999 to February 29, 2000.
Overall, 172 patients were included in the study, of which 159 were attended at the clinic and 13 were hospitalized. A total of 209 individuals presented dermatoses, corresponding to 45.14% of the 381 patients interviewed infected by the retrovirus.
For each patient, the total number of dermatoses present at physical exam was recorded with a subsequent attempt at laboratorial confirmation. The dermatoses were all registered at the time of the first dermatological evaluation.
For the dermatoses classified clinically as having a probable bacterial etiology, cultures for common germs were performed through collection of the exudate or epithelial desquamation when present.
For those of probable fungal etiology, direct mycological exams and culture for fungi were undertaken, whenever there was insufficient epithelial desquamation for collection; except for the cases when the dermatosis involved systemic histoplasmosis, which made it necessary to perform a cutaneous biopsy and anatomicopathological study. For the zoodermatoses, direct microscopic exams were done with tests for the probable agent whenever there was sufficient material for laboratorial confirmation.
Biopsies were performed for all of the neoplastic dermatoses using a number six punch and anatomicopathological study.
For the desquamative diseases included in the clinical classification of noninfectious, non-parasitic and non-neoplastic (miscellaneous) dermatoses, direct microscopic exams with tests for etiological agents were performed in an attempt to differentiate these from dermatoses of other etiologies or to detect parasitic or infectious associations; biopsies of cutaneous-mucous membranes and anatomicopathological study were done in the case of a doubtful diagnostic.
For lesions with oral, anal or genital involvement, complementary invasive exams were not undertaken due to technical difficulties inherent to the service.
All the HIV positive patients (presenting two anti-HIV positive serological tests by the third-generation Elisa method and one positive confirmatory serology through indirect immunofluorescence or Western-Blot) and those presenting dermatoses, whether they were symptomatic or not, with laboratory exams such as CD4+ T lymphocytes count and documented viral load with up to a four-month interval between the collection and the date of the dermatological exam were included.
The dermatoses were diagnosed clinically and classified by clinical and or laboratory methods into seven items, according to Zalla et al.18 and Ray & Gateley,19 as follows: 1) bacterial infections; 2) viral infections; 3) fungal infections; 4) infestations by arthropods; 5) infestations by protozoa; 6) cutaneous neoplasias; and 7) noninfectious, non-parasitic and non-neoplastic dermatoses or those with a poorly defined etiology (miscellaneous).
The severity was evaluated according to the extension of corporal involvement (using the rule of nines for calculating body surface area involved in burns): cephalic segment and neck, 9%; superior members, 9% each segment; hemithorax and lower members, 18% each segment.20
The patients were divided into groups after their first dermatological consultation according to the HIV infection classification in the CDC/1992. The groups were formed by individuals without marked immunosuppression (divided into categories A1, A2, B1, B2, of this classification) and individuals with marked immunosuppression (these were placed in the categories A3, B3, C1, C2, C3 of the same classification, as summarized in box 1.
The lymphocyte count of the peripheral blood was performed with Facscount equipment using flow cytometry technique.21
The method used for quantification of viral RNA, was Nuclisens, licensed by Organon Teknika, Inc., with a computerized quantification Nuclisens reader and detection limit of 80cps/ml.
The results were submitted to statistical analysis. A comparison of the data was established with Student's T test, Fisher and Snedecor F test (Anova), Duncan's test and Chi-square. The 5% minimum significance level was adopted.
The motives for seeking medical help in the first consultation at the Aids reference service or to undergo anti-HIV serology were: 1) medical or paramedical referral (39% of cases); 2) partner seropositive or with Aids (22.1%); 3) clinical complaints or diseases that alerted the individual regarding the possibility of being infected (16.9%); 4) other reasons, not stipulated in the protocol (9.3%); 5) referral by a blood bank (8.1%); 6) suggestion by a seropositive friend or fear of contamination (after sexual relationship without protection) with a sexually transmissible disease (4.7%).
All the 358 dermatoses were registered and classified into 36 clinical diagnoses, as summarized in tables 1 and 2. There was no record of dermatosis caused by protozoa. The occurrence percentage of dermatoses in individuals with and without marked immunosuppression is shown in graph 1.
The Chi-square tests did not reveal any statistically significant difference in the absolute number of dermatoses by similar diagnoses between the groups with and without marked immunosuppression (G2 = 6.35 with four degrees of freedom and p = 0.174).
The most frequent dermatoses were classified as: miscellaneous (seborrheic dermatitis, papular pruritic eruption of HIV, acquired ichthyosis, unguinal hyperchromia, nonspecific eczema, psoriasis, xeroderma, erythroderma, of photoallergic contact dermatitis, granuloma annulare, lupus erythematosus and vitiligo), fungal and viral, which represented 38%, 34.4% and 15.1% of the sample, respectively.
The eight most frequent diagnoses (74.6% of all dermatoses), were: dermatophytosis, seborrheic dermatitis, papular pruritic eruption (PPE of HIV), common wart, candidiasis mucocutaneous, versicolor pityriasis, acquired ichthyosis and herpes simplex.
Forty two patients presented 49 lesions in the mucous membranes at clinical inspection (28.4% of the sample), of which 20 were oral lesions (11 cases of candidiasis, six of oral pilar leukoplasia, one herpes simplex, one herpes zoster and one lymphoma without histological classification), three anal (two cases of condyloma acuminatum and one case of herpes simplex) and 26 genital (eight cases of condyloma acuminatum, seven cases of herpes simplex, four of molluscum contagiosum, three of bacterial balanoposthitis, two cases of balanoposthitis candidiasis, one of bowenoid papulosis and one of vitiligo).
The frequency of the dermatoses, as well as the CD4+ T lymphocytes counts and viral loads for each respective diagnosis are shown in table 1.
A graphical representation of the extension of skin involved by the dermatoses in the patients with and without marked immunosuppression can be seen in graph 2.
The mean value CD4+ T lymphocytes, in absolute numbers (cells/mm3) was of 383.15, and 1,147.00 for the CD8+ T lymphocytes with a mean ratio of CD4/CD8 = 0.33 and viral load of 109,114.05 cps/ml.
The predominant values of CD4+ T lymphocytes were above 200 cells/mm3 (73.8% of the sample), The most frequent viral load values ranged from undetectable to 50,000 cps/ml (71.5% of the sample).
Comparing the viral load data with the values for the CD4+ T lymphocytes, ascertain whether the values are inversely proportional and with a linear relationship, between the logarithms of the two variables.
Comparison of the percentage frequencies of the dermatoses with the distinct groups of immunosuppression, showed a statistically significant difference (p=0.0002), see table 2.
There was a statistically significant difference in the mean values of CD4+ T lymphocytes in patients either with and without marked immunosuppression in all the groups according to number of dermatoses. (see Table 3).
The mean values and standard deviations for the CD4+ T lymphocytes and viral load for the diverse dermatoses are shown in table 4.
Graphic 3 shows the marked variability in the values of the viral load, even after transformation into logarithms.
At the first dermatological consultation, 140 individuals corresponding to 81.4% of the sample, were using antiretroviral drugs. Of these patients, 66 (47.2%) used protease inhibitors in association with other antiretroviral drugs and 74 (52.8%) used antiretroviral associations that did not include protease inhibitors at the time of the dermatological consultation.
The most common associations of antiretroviral medicines were two nucleoside inhibitors of the reverse transcriptase (NTRI) and two NTRI associated to a protease inhibitor
Graphic 4 is a graphical representation of the patients' percentage distribution regarding the use or nonuse of antiretroviral medicines and the number of dermatoses presented.
The result of applying the Student's T test to compare the mean percentage of skin involved by the dermatoses between the patients receiving or not receiving antiretroviral treatment, revealed that there was no statistically significant difference.
In descriptive epidemiology there are basic categories, such as distributions according to time, region and personal attributes in order to identify a general pattern of occurrence in the at-risk groups. Since Aids is an emerging disease, descriptive studies are necessary to indicate the epidemic characteristics in the various populations.22
Descriptive study of case series does not allow, however, the control of bias, which can confuse the association of events with a cause/effect relationship between the same events or statistical findings.
Bias is a systematic error - therefore, it does not arise due to chance - which determines incorrect estimates of associations between exposure and the risk of developing a certain disease.
Bias in analytical studies can be minimized during the planning stage by means of: randomizing the sample (by dividing the sample into groups with identical characteristics for comparison); exclusion (eliminating factors in the sample that are known to confuse the cause/effect relationships) and pairing (relate groups with an increasing degrees of the confounding parameter, or that is, the cases and controls to be compared have confounding factors distributed in an identical manner).
Only 17.7% of the patients with cutaneous disease were not included, as there was no record of the quantification of immune markers, their characteristics were: 26 men and 11 women, with a mean age of 35.3 years, presenting 71 dermatoses (mean 1.9 dermatoses/patient). This low percentage did not compromise the reliability of the results for the frequencies of dermatoses found in this work.
It was decided to obtain the percentage of skin involved by the dermatoses, based on the findings of Smith et al.,13 who describe a close relationship between the severity of the dermatoses and progression of the immunosuppression.
All the information obtained verbally from the patients (marital status, educational level, sexual behavior, origin, home area, profession at the time of the first positive anti-HIV serology, probable means of contamination and motive for seeking specialized Aids service) was subject to bias in remembered information.
The epidemiological characteristics of the sample corresponded to the descriptions of epidemic bulletins in Brazil, mainly in relation to the characteristics of age, sex, means of infection and home area, including a higher frequency of infected bisexuals, in relation to the number of homosexuals in the study. This trend had already been detected in Brazil.24,25
The viral load categories and number of CD4+ T lymphocytes reflected the guides for therapeutics of HIV seropositive individuals25,27 and the publications that evaluated presence of dermatoses in varied levels of CD4+ T lymphocytes.10,12,13,17,18,28-30
A high individual variability was found in the viral load values, hindering their interpretation as a predictor of immunocompetence, although their value as a prognostic of morbimortality and control of therapeutic effectiveness is widely accepted.3,4,7,8,23
Therefore, higher values of standard deviation than the means for viral loads were found in all the groups of dermatoses (Table 4).
The most frequent reasons for seeking specialized attendance at the Aids service point to a low proportion of cases diagnosed by health workers; cohabitation, under risk of contamination, between known partners, and scant knowledge of the infected population regarding the symptoms or even total ignorance of the possibility of asymptomatic seropositive cases.
The finding of a greater frequency of infected individuals with education level between first grade (57% of cases) and second grade (23.3%), compared to illiterate patients (10.5%), is worthy of note, since one would expect a better assimilation of information regarding Aids among individuals with a higher educational level, although this finding is corroborated by the national literature.26
Further studies that extrapolate the behavioral descriptions and analyses will be necessary to clarify this finding in terms of identifying its causes in the context of the Brazilian social vulnerability.31
The finding of a larger number of erythematous squamous dermatoses, included in the miscellaneous group, followed by dermatoses of fungal and viral etiology coincided with world and national reports, in that these three categories of dermatoses include the most frequent skin diseases among those with retroviral infections.2,13,17,32,33
It was not possible, however, to classify the miscellaneous group into scientifically accepted subcategories, since it includes pathologies with varied etiologies and others in which the etiology has yet to be defined.
There were differences in the prevalence of dermatoses according to gender in subjects infected by a retrovirus,30,35 and women presented a lower frequency of Kaposi's sarcoma (three cases involving men and none in women) and oral pilar leukoplasia (five cases in men and one case involving a woman) in this study.
Although it has been reported that T. rubrum is the most frequent dermatophyte among those infected with HIV,17 the finding of a greater frequency of other dermatophytes in the general population has been reported in the national literature, often corresponding to the environmental conditions of the regions studied.36-38
It was observed that T. mentagrophytis was present in most of the dermatophytoses (13 records), against only eight cases of T. rubrum. As for the yeasts, there was growth of colonies in nine cultures.
Descriptive studies, involving immunocompetent and immunosuppressed populations, are necessary to better explain these findings in Rio Grande do Norte.
The high frequency in which S. aureus was isolated in the skin involved by bacterial dermatoses among HIV patients is concordant with world literature17,39,40 and it has been described by Onorato et al.41 The risk factors for acquisition of methicillin-resistant strains in anti-HIV positive individuals are: prior hospitalization, exposure to broad spectrum antibiotics, central venous catheterization and dermatological diseases.
Fifteen patients resistant to penicillin G and/or ampicillin were detected, of which S. aureus was isolated in all cases. Of these, two colonies were also resistant to oxacillin, one colony was not tested for oxacillin and 12 colonies were sensitive to oxacillin. Four colonies of S. epidermidis were isolated and all the colonies were sensitive to oxacillin, but resistant to penicillin G and ampicillin.
The results of the biopsies performed in those cases clinically reported as PPE of HIV, revealed histological patterns described in the literature as predominantly lymphocytic inflammatory infiltrate, with a periannexal and/or superficial and/or profound perivascular location, together with the presence of eosinophiles.
Among cases of inflammatory dermatoses, there are reports of frequent hyperkeratose and/or acanthotic findings and rare granulomas,13 although there was only one case of perforating granuloma annulare.
No reliable information was available regarding duration of the antiretroviral medication use, since many patients had required the use of more than one therapeutic regimen and/or had not used the medicines correctly as prescribed in their records.
Since progress is to be expected in the research into this pandemic, new antiretroviral medicines will be developed, such that studies regarding the behavior of opportunist and co-participating diseases (especially the dermatoses, as they are most frequent in this group of patients) will be important to compare the effectiveness and predictive value of immunological competence among users of the latest antiretroviral drugs.
The epidemiologic characteristics of HIV-infected patients in Rio Grande do Norte did not differ considerably from the characteristics of their counterparts in other Brazilian states.
The most frequent dermatoses: erythematous squamous (included in the miscellaneous group), fungal and viral, correspond to those described in scientific articles.
The sample of patients with a mean count of CD4+ T lymphocytes above 200 cells/mm3 and viral load values lower than 50,000 cps/ml, most of which undergoing antiretroviral therapy, may have positively influenced the findings of similar frequencies of dermatoses among those patients that were or were not using antiretroviral medication.
The variability in the individual markers of immunosuppression and principally in the viral load - whether in the groups with distinct immunosuppression, or users and nonusers of antiretroviral agents may have interfered negatively in the evaluation of the seriousness of the dermatoses.
The numerous factors influencing the immune state of patients under treatment for retrovirus hindered the analysis offence of aggravating risks by introducing a confounding bias which was difficult to control even in an analytical study.
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Tel./Fax: +55(84) 211-9643 / 211-3771
Received in September, 20th of
Approved by the Consultive Council and accepted for publication in November, 05th of 2002.
* Work done at the "Hospital Giselda Trigueiro - Natal/RN".