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Tuberculosis associated to AIDS: demographic, clinical and laboratory characteristics of patients cared for at a reference center in the south of Brazil

Abstracts

BACKGROUND: Synergism between tuberculosis and HIV is responsible for the increased morbidity-mortality rate in AIDS patients. OBJECTIVE: To delineate the profile of patients with tuberculosis and AIDS in the city of Rio Grande by relating demographic, clinical and laboratory data. METHOD: The sample comprised all cases of tuberculosis defined by identification of Mycobacterium tuberculosis that occurred in the AIDS Service of the University Hospital/FURG between September, 1997 and December, 2000, which added to a total of 31 patients confirmed as definite cases of AIDS. Using the Ogawa-Kudoh culture method and the Kinyoun bacilloscopy, 33 clinical pulmonary and extrapulmonary specimens were analyzed. Identification of M. Tuberculosis was made by the usual phenotype methods. The method of proportions was chosen to establish resistance of isolated strains. RESULTS: The mean age was of 33.8±9.9 years, with a man/ woman ratio of 2.87:1 and 80.7% of Caucasians. All patients (n=31) exhibited overall or specific clinical manifestations of turberculosis at the time of suspicion diagnosis. In 20 of the cases risk factors were observed: use of injected drugs, alcoholism, malnutrition, imprisonment. Pulmonary disease occurred in 19 cases, extrapulmonary in 10 and the association of both in two. Lymph node commitment was more frequent among those with extrapulmonary disease. The isolated strains (33) were identified as M. Tuberculosis and 28 were tested and showed sensibility to Isoniazid and Rifampin. CONCLUSION: In AIDS patients, tuberculosis appeared with various clinical manifestations, jeopardizing both men and women of less favored social conditions while at a fully productive stage of their lives.

Tuberculosis; Tuberculosis; Acquired immunodeficiency syndorme; Mycobacterium tuberculosis


INTRODUÇÃO: A sinergia entre a tuberculose e o vírus da imunodeficiência humana é responsável pelo aumento da morbi-mortalidade dos pacientes com AIDS. OBJETIVO: Delinear o perfil de pacientes com tuberculose e AIDS na cidade de Rio Grande (RS) relacionando dados demográficos, clínicos e laboratoriais. MÉTODO: A amostra foi constituída por todos os casos de tuberculose confirmados pelo isolamento de Mycobacterium tuberculosis ocorridos no Serviço de AIDS do Hospital Universitário/FURG entre setembro de 1997 e dezembro de 2000, em 31 pacientes reportados como casos definidos de AIDS. Foram examinados 33 materiais clínicos pulmonares e extrapulmonares através da cultura pelo método de Ogawa-Kudoh e da baciloscopia pelo Kinyoun. A identificação de M. tuberculosis foi feita pelos métodos fenotípicos usuais. Para determinação da resistência das cepas isoladas foi empregado o método das proporções. RESULTADOS: A média de idade foi de 33,8 ± 9,9 anos, com uma relação homem/mulher de 2,87:1. Eram brancos 80,7% dos pacientes. Todos os pacientes apresentavam manifestações clínicas gerais e/ou específicas de tuberculose no momento da suspeita diagnóstica. Em 20 deles foram constatados fatores de risco: uso de droga endovenosa, alcoolismo, desnutrição, encarceramento. A doença pulmonar ocorreu em 19 casos, a extrapulmonar em 10 e a associada em 2 deles. Entre aqueles com a forma extrapulmonar, predominou o comprometimento ganglionar. As 33 cepas isoladas foram identificadas como M. tuberculosis, e 28 mostraram sensibilidade à isoniazida e à rifampicina. CONCLUSÃO: A tuberculose nos pacientes com AIDS apresentou-se com manifestações clínicas variáveis, comprometendo homens e mulheres em condições sociais desfavoráveis, em plena fase produtiva de suas vidas.

Tuberculose; Tuberculose; Síndrome da imunodeficiência adquirida; Mycobacterium tuberculosis; Indicadores de morbi-mortalidade


ORIGINAL ARTICLE

Tuberculosis associated to AIDS: demographic, clinical and laboratory characteristics of patients cared for at a reference center in the south of Brazil * * Study carried out in the Mycobacteria Laboratory of the Pathology Department of the Fundação Universidade Federal do Rio Grande (UFRG), RS; Laboratório Central (LACEN), Secretaria da Saúde e Meio Ambiente, Porto Alegre, RS.

Maria Marta Santos Boffo; Ivo Gomes de Mattos; Marta Osório Ribeiro; Isabel Cristina de Oliveira Neto

Correspondence Correspondence Rua Marechal Deodoro, 278 96211480, Rio Grande, RS Phone: (53) 2326270, (53) 99715371 e-mail: dpammsb@super.furg.br

ABSTRACT

BACKGROUND: Synergism between tuberculosis and HIV is responsible for the increased morbidity-mortality rate in AIDS patients.

OBJECTIVE: To delineate the profile of patients with tuberculosis and AIDS in the city of Rio Grande by relating demographic, clinical and laboratory data.

METHOD: The sample comprised all cases of tuberculosis defined by identification of Mycobacterium tuberculosis that occurred in the AIDS Service of the University Hospital/FURG between September, 1997 and December, 2000, which added to a total of 31 patients confirmed as definite cases of AIDS. Using the Ogawa-Kudoh culture method and the Kinyoun bacilloscopy, 33 clinical pulmonary and extrapulmonary specimens were analyzed. Identification of M. Tuberculosis was made by the usual phenotype methods. The method of proportions was chosen to establish resistance of isolated strains.

RESULTS: The mean age was of 33.8±9.9 years, with a man/ woman ratio of 2.87:1 and 80.7% of Caucasians. All patients (n=31) exhibited overall or specific clinical manifestations of turberculosis at the time of suspicion diagnosis. In 20 of the cases risk factors were observed: use of injected drugs, alcoholism, malnutrition, imprisonment. Pulmonary disease occurred in 19 cases, extrapulmonary in 10 and the association of both in two. Lymph node commitment was more frequent among those with extrapulmonary disease. The isolated strains (33) were identified as M. Tuberculosis and 28 were tested and showed sensibility to Isoniazid and Rifampin.

CONCLUSION: In AIDS patients, tuberculosis appeared with various clinical manifestations, jeopardizing both men and women of less favored social conditions while at a fully productive stage of their lives.

Key words: Tuberculosis/epidemiology. Tuberculosis/ complications. Acquired immunodeficiency syndorme/tuberculosis. Mycobacterium tuberculosis/indicators of morbidity and mortality.

Abbreviations used in this paper:

AIDS – Acquired immunodeficiency syndrome

HIV – Human immunodeficiency virus

WHO – World Health Organization

FURG – Fundação Universidade Federal do Rio Grande

UH – University Hospital

95% CI – 95% confidence interval

Introduction

Synergism between tuberculosis and human immunodeficiency virus (HIV) is responsible for the increased morbidity-mortality rate in AIDS patients.(1) In 1981, when the first case of AIDS was diagnosed, it was estimated that one third of the world population was infected by Mycobacterium tuberculosis. Until then, the majority of infections caused by M. tuberculosis remained latent in their hosts, due to an efficacious cellular immune response. However, the dissemination of HIV infection throughout the world has altered human defense mechanisms against tuberculosis. Infection with HIV has therefore become the primary risk factor for the evolution of latent infections caused by M. tuberculosis.(2) It is estimated that 500,000 HIV-infected individuals live in Latin America, where the incidence of tuberculosis has reached epidemic proportions. For various urban areas, including some in Brazil, the World Health Organization (WHO) has stated that rates of tuberculosis constitute “an emergency”.(3)

The city of Rio Grande in the state of Rio Grande do Sul is a port and industrial center in the south of Brazil and is located in a region where there is a high prevalence of tuberculosis.(4) The city also ranked sixth in the state in the number of AIDS cases reported between 1980 and 2002.(5) It therefore creates an ideal environment for the appearance of co-infections with tuberculosis and AIDS.

The objective of this study was to delineate, based on demographic, clinical, and laboratory data, the profile of a population of AIDS patients with tuberculosis in the city of Rio Grande.

Methods

The sample comprised all patients examined in the Serviço de AIDS of the Hospital Universitário of the Fundação Universidade Federal do Rio Grande (HU/FURG) between September 1997 and December 2000 and diagnosed with tuberculosis through isolation of M. tuberculosis in laboratory testing. A total of 31 patients were included. All patients were classified as AIDS patients, as defined by the HIV and AIDS classification system devised by the Centers for Disease Control and Prevention.(6) Information on patients was collected either in direct interviews or from medical records and was transferred to specific forms by the attending physician. The diagnosis of HIV infection was confirmed by positive serology, using either immunofluorescence or Western Blot test. Serological tests were performed either in the Laboratório Central da Secretaria da Saúde e Meio Ambiente do Rio Grande do Sul or in the Laboratório de Apoio à AIDS of the HU/FURG.

There was clinical suspicion or radiological evidence of tuberculosis in all 31 patients studied. Therefore, smear microscopy and culture of 33 samples were performed. The samples were obtained from pulmonary sites through sputum collection or bronchoalveolar lavage and from extrapulmonary sites through collection of ascitic or pleural fluid, or through ganglion or liver biopsy. Kinyoun’s stain was used for screening smears for acid-fast bacilli.(7) Ogawa-Kudoh(8) culture medium and Ogawa culture medium enriched with thiophene-2-carboxylic acid hydrazide and p-nitrobenzoic acid(9) were used for primary isolation and initial identification of M. tuberculosis. The presence of M. tuberculosis was confirmed by niacin test according to the recommendation of the Tuberculosis Bacteriology Handbook.(10) In order to test isolated M. tuberculosis strains and determine profiles of sensitivity and resistance to isoniazid and rifampin, the proportion method (indirect technique),(10,11) which is considered the standard,(12) was used.

The statistical analysis included calculation of means and standard deviations for continuous variables. For categorical variables, percentages were calculated and, for some, the 95% confidence interval (95% CI) was determined.

Results

The demographic characteristics of the patients are summarized in Table 1. Males outnumbered females by 2.87 to 1. There were also more Caucasians (80.7%). The mean age was 33.8 ± 9.9 (range, 19 to 65). Age distribution indicates there was a greater number of cases in the 25-44 age bracket. All patients were employed as unskilled laborers or were involved in occupations that do not require higher education. Most patients (90.3%) lived in the city, mainly on the outskirts.

All of the 31 patients suspected of having tuberculosis presented one or more general symptoms, the most common of which was fever (in 64.5%), followed by weight loss, asthenia and night sweats (Table 2). Cough (with or without expectoration) was observed in 32.3% of cases. Chest pain was reported by 1 patient whose chest X-ray revealed pleural effusion. Of the 3 patients who reported abdominal pain, ascites was revealed during physical examination in 2. Lymph node enlargements (submandibular, axillary, supraclavicular and generalized) were found in 9 patients (29%). Of these, 6 (19.4%) had lymph node tuberculosis, 1 (3.2%) had pulmonary tuberculosis, and 2 (6.4%) had hematogenous dissemination. Patients with lymph node enlargement also presented one or more additional general symptoms.

In 20 (64.5%) of the patients, risk factors such as injection drug use, alcoholism, malnutrition and imprisonment were present (Table 3). Approximately half of the patients studied were injection drug users (48.4%; 95% CI = 30.2 to 66.9), and approximately one-third were alcoholics (35.5%; 95% CI = 19.2 to 54.6). Risk factors were absent in Approximately one third of the patients denied any tuberculosis risk factors.

Smear microscopy was positive in 33.3% of the various samples collected (Table 4), and was used to confirm the initial diagnosis of tuberculosis of 11 patients. The isolated strains from the 31 cases under evaluation were all identified as M. tuberculosis. The pulmonary form of the disease was identified in 19 patients (61.3%; 95% CI = 42.2 to 78.2). In 13 patients (41.9%), M. tuberculosis was isolated in bronchoalveolar lavage samples, and, in 6 patients (19.4%) it was isolated in sputum samples. Extrapulmonary tuberculosis was diagnosed in 10 patients (32.3%; 95% CI = 16.7 to 51.4), with lymph node involvement in 7 (22.6%), peritoneal involvement in 1 (3.2%), pleural involvement in 1 (3.2%) and dissemination in 1 (3.2%). Extrapulmonary involvement was also found in 2 patients (6.5%; 95% CI = 0.8 to 21.4) patients with pulmonary tuberculosis; 1 presenting superficial lymph node involvement, and 1 presenting liver involvement related to dissemination of the disease (Table 5).

In 28 patients, the M. tuberculosis strains isolated tested positive for sensitivity to both isoniazid and rifampin. Of those 28 patients, 22 (78.6%) were treatment naive, 5 (17.8%) had recently completed treatment or had used antituberculosis drugs irregularly. We were unable to determine treatment history for 1 patient (3.6%).

Discussion

In the group of patients studied, there was a predominance of males, which is in accordance with data from other studies carried out in various regions of Brazil.(13,14) This may be related to the 1.5:1 to 2.1:1 male/female ratio among tuberculosis cases reported to the WHO.(15) On the other hand, it could be related to the prevalence of males among AIDS cases, a 2:1 ratio in Brazil in 2000.(5) A combination of biological and social factors may be responsible. Such factors determine physiological differences, diversity of behavior, expectations, and activities that coexist in a social, economic, and cultural context. The mean age of the patients in this study was approximately 30, which is in accordance with the findings of other studies.(13,14,15) The high prevalence of tuberculosis and AIDS in this age group may be linked to the lifestyle of young adults, who are more permissive and promiscuous, resulting in higher exposition to M. tuberculosis and HIV.(15) The higher prevalence of Caucasians (80.7%) in the study sample may be related to the race profile of the population in Rio Grande do Sul, of which Caucasians constitute 87.3%,(16) rather than to a racial predisposition to tuberculosis. Worldwide, the prevalence of tuberculosis among individuals of African descent is twice as high as that seen among Caucasians.(17) It must be taken into account that the highest rates of tuberculosis are found in Africa, where 31% of adult tuberculosis cases involve co-infection with HIV.(18) The relationship of this information to the socioeconomic conditions in Africa may be more relevant than its relationship to ethnicity. However, a study carried out in the USA in 1990 reported that the relative risk of infection by M. tuberculosis was twice as high for African-Americans as for Caucasians.(17) In our study, the analysis of occupational status and origin revealed that the co-infection affected people of low socioeconomic status, which is in accordance with the “pauperization” phenomenon seen in Brazil. Between 1991 and 2001, more than 50% of all adult AIDS patients of both genders were individuals with little schooling.(5)

Infection with HIV is considered the most significant risk factor for the development of tuberculosis. In 1997, it was estimated that approximately 150,000 HIV-infected Brazilians had been co-infected with tuberculosis within the previous 5 years.(19) In the present study, the predominant risk factor for such co-infection was found to be the use of injection drugs (48.4%), which may indicate the significance of this risk factor in relation to HIV infection in our country.(20) In 1997, such a relationship was reported in Spain, and, to some extent, the lifestyle of young adults was conducive to it.(15) The second most prominent risk factor in our study was alcoholism (35.5%). In another study of co-infected patients, alcoholism was found to be the most significant risk factor (25%), followed by injection drug use (9.1%).(13)

Other aspects to be discussed are the changes in the clinical manifestations and presentations of tuberculosis reported in the literature since 1980s, which is associated with the advent of AIDS. The distribution of signs and symptoms in the patients in this series was similar to that reported in previous studies conducted in various regions.(2,21) When evaluating tuberculosis in patients with HIV, physicians must take into consideration the possibility of atypical clinical manifestations or radiography findings. In order to confirm a diagnosis of tuberculosis in HIV-infected patients, it is therefore necessary to perform anatomopathological and microbiological tests in samples taken from various anatomical sites.(19)

In 14 of the patients presenting pulmonary involvement, there was no expectoration, and the diagnosis of tuberculosis was confirmed by isolation of M. tuberculosis through bronchoalveolar lavage. This procedure is responsible for an increase of 66.6% in the diagnosis of pulmonary disease and has been reported as a safe and effective method for the diagnosis of mycobacteriosis.(13,22) The efficiency of mycobacteria detection by culture and smear microscopy in extrapulmonary samples varies according to the anatomical site involved and the type of sample collected for examination (biopsy, aspirate, fluid from cavities, etc.)(19,23) Among the extrapulmonary samples tested in this study, ganglion biopsy presented the highest diagnostic yield. The resection of the ganglion that seemed to be the most affected and the most accessible has been recommended. In some series, positive microscopy results were obtained from 100% of ganglion biopsy samples. Therefore, some authors have considered that more positive microscopy results may be obtained from ganglion biopsy samples in patients infected by HIV(23). Hepatic biopsies, bone marrow biopsies and blood samples have been referred to as the materials that are most sensitive in the diagnosis of tuberculosis with hematogenous dissemination.(22,23) In a previous study, 15 hepatic biopsy samples were analyzed and M. tuberculosis was isolated in 7. Of those 7, microscopy results were positive in 4 and histopathology revealed granuloma in 6.(24) In the present study, the 2 patients presenting hematogenous dissemination were diagnosed through isolation of M. tuberculosis in hepatic biopsy samples.

In the present study, the predominant form of tuberculosis was the exclusively pulmonary form (19/31). Pulmonary/extrapulmonary or exclusively extrapulmonary tuberculosis was diagnosed in 12 patients, and, among those 12, the site of infection was most commonly ganglial. The fact that tuberculosis is more likely to be diagnosed with certainty through laboratory testing may explain the low incidence of extrapulmonary tuberculosis found in our study. In a previous study, a diagnosis of extrapulmonary tuberculosis was confirmed in 17.56% of samples taken from extrapulmonary sites in 74 patients examined at the Serviço de AIDS in Rio Grande.(25) In studies conducted in other states (in the cities of Rio de Janeiro and São Paulo), lymph node tuberculosis was found to be predominant in cases of AIDS patients with extrapulmonary tuberculosis,(21,26) although a study conducted between 1995 and 1998 in the city of Brasília found no influence of HIV infection on the clinical presentation of new tuberculosis cases.(27) In Spain, Castilla et al. found no significant difference between pulmonary and extrapulmonary tuberculosis incidence in HIV-positive patients.(15) It is important to mention that, in our study, extrapulmonary samples were only collected if there was clinical suspicion of extrapulmonary involvement, and no extrapulmonary samples were collected from patients whose pulmonary samples were positive for mycobacteria. This may explain why there were few patients that were diagnosed with pulmonary/extrapulmonary tuberculosis. This may also be the reason why other studies conducted in Brazil have reported low rates of this form of the disease.

In all of the patients studied, M. tuberculosis was the bacterial species responsible for tuberculosis infection. This knowledge was crucial to determining the initial treatment regimen chosen for HIV-positive or AIDS patients (2RHZ/7RH).(19) This regimen is recommended by the Health Department and is extremely efficacious, having a very low failure rate for M. tuberculosis. Inadequate adherence to this treatment regimen, frequently due to non-compliance by patients, has been considered an important risk factor for the appearance of strains resistant to isoniazid and rifampin. In Brazil, recent studies have also incriminated poor infrastructure and alcoholism as determinant factors for the development of multi-drug resistant tuberculosis.(28) Proper treatment and patient adherence is considered the most simple and inexpensive method for the prevention of developing resistant strains of M. tuberculosis. However, improving the quality of life of the population is also important. In the present study, the isolated strains were not resistant to isoniazid or rifampin, although 5 patients had been previously treated for tuberculosis. In a parallel evaluation of 72 M. tuberculosis strains isolated from non-AIDS patients in Rio Grande, 4 (5.56%) were resistant to isoniazid, 2 (2.77%) were resistant to both isoniazid and rifampin, and 4 strains were isolated from patients who had previously been treated for tuberculosis.(29)

In this study, we demonstrated higher co-morbidity when tuberculosis is atypical in presentation. Therefore, we recommend that medical teams increase the level of clinical suspicion and number of laboratory tests performed during examinations of young adults, especially those in their prime, that come from low socioeconomic backgrounds.

References

Submitted: 24 July 2003.

Accepted, after revision: 28 November 2003.

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  • Correspondence
    Rua Marechal Deodoro, 278
    96211480, Rio Grande, RS
    Phone: (53) 2326270, (53) 99715371
    e-mail:
  • *
    Study carried out in the Mycobacteria Laboratory of the Pathology Department of the Fundação Universidade Federal do Rio Grande (UFRG), RS; Laboratório Central (LACEN), Secretaria da Saúde e Meio Ambiente, Porto Alegre, RS.
  • Publication Dates

    • Publication in this collection
      08 June 2004
    • Date of issue
      Apr 2004

    History

    • Accepted
      28 Nov 2003
    • Received
      24 July 2003
    Sociedade Brasileira de Pneumologia e Tisiologia SCS Quadra 1, Bl. K salas 203/204, 70398-900 - Brasília - DF - Brasil, Fone/Fax: 0800 61 6218 ramal 211, (55 61)3245-1030/6218 ramal 211 - São Paulo - SP - Brazil
    E-mail: jbp@sbpt.org.br