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HIV Prevalence Among Pulmonary Tuberculosis Patients in Guangxi, China

Wang, Liyan MD, MS*; Liu, Wei MD, MS; Wang, Lu MD, PhD*; Wang, Yan MD, MS; Wu, Zunyou MD, PhD§

JAIDS Journal of Acquired Immune Deficiency Syndromes: February 2010 - Volume 53 - Issue - p S61-S65
doi: 10.1097/QAI.0b013e3181c7db2e
Supplement Article

Objective: To determine the HIV prevalence rate among tuberculosis (TB) patients in Guangxi, China.

Methods: Stratified cluster sampling and systematic sampling methods were used to select 16 clinics from which pulmonary TB patients were recruited to participate in this study. Two thousand three hundred pulmonary TB patients provided information on sociodemographic characteristics, HIV-related knowledge and high-risk behaviors, and method of TB diagnosis. Five-milliliter blood sample from the regular TB check up was retained and tested for HIV antibody.

Results: HIV prevalence among pulmonary TB patients was 0.5% (12 of 2300). There was statistical difference in HIV prevalence neither between urban and rural nor between male and female patients; however, TB patients from higher HIV prevalence areas had a higher rate of HIV infection than TB patients from a lower HIV prevalence areas for both rural or urban areas (0.8% vs. 0, χ2 = 7.49, P < 0.01).

Conclusions: HIV prevalence is higher among pulmonary TB patients than among the general population in Guangxi. Program to address the dual infections of HIV/TB are needed.

From the *Division of Epidemiology, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; †Center for Disease Control and Prevention, Guangxi Zhuang Autonomous Region Center for Disease Control and Prevention, Nanning, Guangxi, China; and ‡Division of HIV/AIDS, Harbin Center for Disease Control and Prevention, Harbin, Heilongjiang, China; §National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China.

Supported by fund from the National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention; and Liyan Wang was supported by the China Multidisciplinary AIDS Prevention Training Program with NIH Research Grant # U2R TW06918 funded by the Fogarty International Center, National Institute on Drug Abuse, and the National Institute of Mental Health (China ICOHRTA, with Principal Investigator Z. Wu).

Correspondence to: Zunyou Wu, MD, PhD, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 27 Nanwei Road, Beijing 100050, China (e-mail:

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Immunosuppression as a result of HIV infection increases the frequency and speed of progression from latent tuberculosis (TB) infection to active TB.1,2 According to the World Health Organization, TB is one of the major causes of death among HIV-infected people, and TB/HIV coinfection has been found to reduce the effectiveness of directly observed therapy treatment of TB.3,4 Concern over growing HIV-driven epidemics of TB has galvanized global consensus on this issue; however, large-scale implementation of public health strategy to jointly address HIV/TB coinfection.5,6

China has been identified as one of the countries where a rapidly increasing HIV epidemic could fuel an epidemic of TB.6,7 China is one of 22 countries with a high TB burden and has a growing HIV epidemic. In 2000, it was estimated that approximately 9% (range: 7%-12%) of all new TB cases in adults worldwide (of which 31% were in Africa and 26% in the United States) were attributable to HIV infection, as were 12% of the 1.8 million deaths from TB, crippling already overburdened health care resources.6,8

A 2000 national TB epidemiology survey conducted in China reported overall TB prevalence of 367 cases per 100,000 (0.0036%), with an estimated 4.5 million active pulmonary TB patients and 1.5 million new infections a year.9,10 At present, the HIV epidemic in China continues to gain momentum after the first detection of a group of infected injecting drug users in southern China in 1989; by 1998, HIV infection had been detected in every province and by 2007, an estimated 700,000 people were thought to be living with HIV/AIDS.11 Although HIV in China disproportionately affects groups such as commercial sex workers and their clients, injecting drug users and men who have sex with men,11 people infected with TB tend to be from poor socio-economic backgrounds with limited access to information and adequate health services, such as farmers or laborers.12 The overlap among the populations vulnerable to HIV and TB infections points to the systematic challenges in controlling the twin epidemics, which must address issues of health care access and provision of information on prevention methods.

Should the TB/HIV coinfection rate increase, it is anticipated that providing comprehensive HIV/AIDS care and support to HIV-positive TB patients such as antiretroviral therapy, and the monitoring and management coinfection cases,13 will be made more difficult. On top of this, health care services in poor areas of China suffer from a lack of infrastructure, aging equipment, and a shortage of adequately trained healthcare workers, resulting in additional overburdening of already strained health care institutions.14

HIV prevalence in TB patients can be used as an indicator of the degree of spread of HIV into the general population. This information is also important for the provision of comprehensive HIV/AIDS care and support.13 A routine TB-HIV integrated surveillance system to monitor and evaluate the implementation of HIV testing and provision of HIV care to TB patients needs to be established. China does not have such surveillance and will require basic information to establish this system. As such, there is little published or existing data available on HIV infection rates among TB patients in China.

Guangxi Autonomous Region bears an unusually high burden of pulmonary TB and HIV/AIDS in China. In 2000, Guangxi had a TB prevalence rate of 650 of 100,000,15 and the HIV prevalence in 2003 was 0.1% of the general population.16 The purpose of this article is to determine the HIV prevalence rate among TB patients in Guangxi.

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Data Collection

Data were collected between December 2005 and February 2006, and a total of 2300 participants were recruited as study subjects. A stratified cluster sampling method was used for selecting pulmonary TB patients. Counties were stratified into 4 types according to whether an area was urban or rural and whether the number of cumulative reported HIV/AIDS cases was above or below the 2004 provincial-wide by-county median figures for respective type of county (rural, urban). As can be seen in Figure 1, area 1 sites were identified as rural with above average HIV; area 2 sites were rural with below average HIV; area 3 sites were urban with above average HIV; and area 4 were urban areas with below average HIV (Fig. 1). Of a total of 86 TB treatment clinics administered by the Guangxi Center for TB Prevention and Control, 36 were identified in area 1, 36 in area 2, 7 in area 3, and 7 in area 4.



The second stage of sampling consisted of selecting clusters of patients from each area. Six clinics were systematically sampled from each of areas 1 and 2, and 2 clinics were from each of areas 3 and 4 (Fig. 1), for a total of 16 clinics. Consecutive sampling methods were used within the cluster to enroll patients. Trained clinicians at each selected clinic screened newly diagnosed and existing pulmonary TB patients for study eligibility. Eligible patients who consented to participate in the study answered questions regarding sociodemographic characteristics, medical history, and HIV/AIDS-associated knowledge. Each subject also provided a blood sample for HIV testing.

Pulmonary TB patients were diagnosed in at least 1 of the following ways: (1) sputum TB tested positive (smear examination or bacillus incubation); (2) sputum tested TB negative, but active TB symptoms were identified through X-RAY; (3) pathological diagnosis of TB; (4) suspected pulmonary TB patient if other pulmonary diseases were ruled out after a follow-up X-RAY; and (5) person suffered from TB-related pleuropneumonia (except for thorax hydrocele, which can be caused by other infections).17

During a regular follow-up visit, blood specimen is taken to test hepatofunction and hemogram. The remainder of the blood sample was used to test for HIV. HIV-positive cases were confirmed by Western blot method (test kit made by Genelabs Technologies Inc, Cavendish, Singapore) after testing positive for HIV antibody using 2 different types of enzyme-linked immunosorbent assays (the first enzyme-linked immunosorbent assay test kit was made by Beijing WANTAI Biological Pharmacy Company, Beijing, China, and the second was made by Livzon Group Reagent Factory, Zhuhai, China). All samples were prepared according to Genelabs Technologies Inc's instructions and blind tested at the Guangxi Center for Disease Control and Prevention (CDC) using Microsoft Excel (Microsoft, Redmond, WA) for automated test result interpretation.18

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Data Analysis

All survey data were double entered at the Guangxi CDC and validated using Epidata 3.0 (The EpiData Association, Odense, Denmark). Data analysis was conducted with SPSS10.0 for Windows (SPSS Inc, Chicago, IL). All descriptive data were described using frequencies and median values. χ2 tests of association were conducted to compare categorical variables.

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Quality Control

Standardized protocols and questionnaires were used in each study site by the interviewers to collect data during the survey period. The interviewers were TB clinic doctors and were given interview training by TB and HIV experts from the China CDC (National) and the Guangxi CDC (Provincial). During the survey, 2 supervisors from the China CDC and the Guangxi CDC periodically monitored data collection either in person or via the telephone.

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The study protocol was approved by the institute review board at the National Center for AIDS/STD Control and Prevention, Chinese CDC.

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Sociodemographic Characteristics

A total of 2300 participants were recruited. The mean age was 41.8 (SD, 17.6) years (Table 1). The majority were male (68.7%), of Han ethnicity (69.2%), married or living with their regular partner (72.2%), and had at least 9 years of schooling (72.3%). The most common occupations were farmers and laborers.



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HIV/AIDS-Related Behaviors and Knowledge

Among the 2300 subjects, 17 (0.7%, 95% CI: 0.4% to 1.2%) participants reported a history of injecting drug use, and 53 (2.3%, 95% CI: 1.7% to 3.0%) participants reported at least 1 lifetime commercial sex experience (either as a sex worker or a client). Sixty-nine (3.0%, 95% CI: 2.3% to 3.8%) participants had ever received blood transfusions, and 57 participants (2.5%, 95% CI: 1.9% to 3.2%) had ever received blood products. Five men (0.3%, 95% CI: 0.1% to 0.7%) reported sex with other men.

The United Nations General Assembly Special Session on HIV/AIDS indicators were used to test knowledge of HIV prevention methods. Participants were assigned a score based on the percentage of questions answered correctly. Using this composite indicator, 39 (1.7%) received a score of 100%; and the percentage of respondents with perfect scores for areas 1, 2, 3, and 4, were 1.4%, 1.1%, 3.4%, and 1.4%, respectively (Table 2).



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HIV Prevalence

Twelve participants tested positive for HIV, for a study sample prevalence rate of 0.5% (95% CI: 0.3% to 0.9%). There was no significant difference in HIV prevalence between urban (0.5%, 95% CI: 0.1% to 1.5%) and rural (0.5%, 95% CI: 0.2% to 1.0%) participants. However, HIV prevalence among pulmonary TB cases selected in the 2 areas where the cumulative number of HIV/AIDS cases was above the provincial median (0.8%, 95% CI: 0.4% to 1.5%) was higher than the cases selected from the areas where the cumulative number of HIV/AIDS cases was below the provincial median (0, one sided 97.5% CI: 0% to 0.4%), χ2 = 7.49, P < 0.01). This finding indicates that TB patients in high HIV settings are more likely to have HIV than TB patients in low HIV settings. No significant difference was found with regard to other variables, including ethnicity, gender, age, or occupation (Table 3).



Among the 12 coinfection cases, 11 were males with ages ranging 20-49. Ten of the cases were either from the Han ethnic group, had completed less than 9 years of education, or were farmers. Seven of the cases (58.3%) were married. Nine coinfected participants (75%) were diagnosed with pulmonary TB with sputum negative or no sputum tests (Table 3). This result implies that when HIV-positive people are screened for pulmonary TB, diagnosis should not focus solely on sputum-positive or incubation-positive methods of diagnosis.

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The 0.5% HIV prevalence found among pulmonary TB patients is markedly higher than the provincial average of 0.1% in Guangxi. This finding is consistent with results reported in African countries.19,20 The HIV/TB coinfection rate in our study is lower than the national HIV/TB coinfection rate of 4.3% in Vietnam, a neighboring country with a similar national HIV prevalence rate as China but with a higher TB rate. The same rate was even higher in the capital of Ho Chi Minh City: TB patients were found to have HIV prevalence of 9.8% in 2005.21,22

The finding of 0.5% HIV prevalence among TB patients is comparable with similar surveys conducted among TB patients in Hunan and Henan, where HIV/TB coinfection rates of 0.96% and 0.39%, respectively, were found among TB patients.23,24 A study conducted in 4 counties of Hebei, a province with lower HIV but high TB prevalence, found 0% HIV infection among its TB patients, although another conducted in a county in Henan found this same rate to be 5.1%.25,26

According to the results of this study, HIV/TB coinfection prevalence is 0% in Guangxi in areas with a HIV prevalence rate below the provincial median for rural and urban areas. This suggests the most efficient use of resources would be to establish TB/HIV coinfection sentinel surveillance sites in high HIV prevalence areas, as such sites will be more efficient at finding coinfections.

This study had several limitations. First, the nonprobability sampling methods may have resulted in a biased sample; however, some researchers have found bias from cluster sampling to be minor compared with estimates derived using simple random sampling.27,28 Second, “self-reporting” bias may have underestimated more sensitive information such as drug use and commercial sex.

HIV-related TB not only fuels the world-wide TB epidemic and increases the burden of TB control and prevention, but TB has also become the leading cause of death in people living with HIV/AIDS. The World Health Organization suggests countries with limited resources and in the planning stages of establishing a HIV/TB sentinel surveillance system should periodically conduct HIV screening among pulmonary TB patients.3 However, this study suggests the coinfection prevalence of TB and HIV in Guangxi is not as high as other countries with high HIV and TB burdens where coinfection rates between 1.5% and 9% have been reported.29 Our study findings suggest TB/HIV coinfection sentinel surveillance sites among pulmonary TB patients should be limited to the areas with a high HIV prevalence in China.

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The authors gratefully acknowledge the help of Qiuying Zhu, Weijiang Lu, and all the other public health officers in Guangxi. CDC, who participated in this survey and the doctors in 16 TB clinics for assisting in collecting the data. We would also like to thank Naomi Juniper and Adrian Liau for reviewing and editing the article.

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China; coinfection; HIV; tuberculosis

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