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Risk of HIV Transmission Within Marriage in Rural China: Implications for HIV Prevention at the Family Level

Liu, Hongjie PhD*; Detels, Roger MD; Li, Xiaoming PhD*; Stanton, Bonita MD*; Hu, Zhi PhD; Yang, Hongmei PhD*

Sexually Transmitted Diseases: July 2005 - Volume 32 - Issue 7 - p 418-424
doi: 10.1097/01.olq.0000170446.01789.4e
Article
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Background: Little is known about HIV transmission at the family level in China.

Goal: We examined the risks for HIV transmission between husbands and wives and from parents to children in a rural area where HIV spread among former commercial blood donors.

Study: A cross-sectional study was conducted among 605 (302 couples) marriage license applicants.

Results: More males (64.6%) than females (52.1%) reported having had premarital sex and multiple sex partners (12.6% and 6.9%, respectively). Among those having had multiple sex partners, 8.5% reported often or always using condoms. Only 36.8% of the couples agreed that they would not plan to have a baby after knowing the status of HIV infection. Approximately 43% of the couples agreed that they would use condoms consistently if 1 of them were HIV-positive.

Conclusions: There is an urgent need for national programs to prevent HIV infection within couples in rural areas.

A study conducted in an HIV-infected rural area in China found that the risks of HIV transmission between husbands and wives and from parents to children exist among newly married couples.

From the *School of Medicine, Wayne State University, Detroit, Michigan; the †School of Public Health, University of California, Los Angeles, California; and the ‡School of Health Administration, Anhui Medical University, Hefei, China

The authors thank Kathleen Meert and Wendy Aft for editing the manuscript. Special thanks to all participants in the study.

This study was supported by a grant from the International Society for Infectious Diseases (ISID) to Hongjie Liu.

Correspondence: Hongjie Liu, PhD, MS, Assistant Professor, Prevention Research Center, School of Medicine, Wayne State University, 4201 St. Antoine, UHC-6D, Detroit, MI 48201-2196. E-mail: hongjie@med.wayne.edu.

Received for publication September 14, 2004, and accepted December 14, 2004.

ASIA IS NOW HOME TO some of the fastest-growing AIDS epidemics in the world.1 As estimated by UNAIDS, 7.4 million Asian people are living with HIV. There is particular concern about the epidemic in China; although the overall prevalence rate among the adult population is still low (0.1% in 2003), the rate of spread of the epidemic is among the highest in the world.2,3 In China, there is a high rate of HIV among intravenous drug users.4 China also experienced an epidemic among commercial blood donors in the poor rural areas of the central provinces.5,6 HIV infection among former commercial plasma donors was initially reported in Anhui Province, but more serious problems were reported later from Shanxi, Shaanxi, Hebei, Gansu, Hubei, and Henan.7 Although a safe blood supply has been secured in the urban areas, there are still problems with safe collection and use of blood in the rural areas.2

In most Asian countries, HIV epidemics follow a chain of transmission.8,9 HIV spreads first among injecting drug users; subsequently, transmission occurs among sex workers. Clients of sex workers then transmit HIV to their female sexual partners. Most women infected in Asia have been monogamous wives or regular partners. Through maternal infection, women living with HIV transmit the virus to their children in the final link of the chain. The spread of HIV in China has reached the stage of mother-to-child transmission. Since the first case of mother-to-child transmission was reported in 1995, the proportion has increased from 0.1% of the total reported HIV-positive cases in 1997 to 0.4% in 2002.10 In Yunnan and Xinjiang, the HIV prevalence among pregnant women in certain areas reached 1.3% and 1.2%, respectively, similar to levels of high-prevalence neighboring countries.10 Studies in China have confirmed that HIV transmission is occurring at the family level. Two recent studies conducted among former commercial blood donors show that the rate of HIV sexual transmission among discordant couples is 11%11 and the rate of mother-to-child transmission is 38%.12

HIV transmission at the family level is not a random event, but rather is determined by risky behaviors practiced by each partner of a couple. Transmission can therefore be prevented or controlled by behavioral intervention programs. It is important, however, to understand risk factors for acquiring HIV within marriage in China to develop effective intervention programs. Little information is currently available about the extent and correlates of HIV-related knowledge, perception of vulnerability to HIV infection, unsafe sex behaviors, and effective risk-reduction strategies specific to this population. For example, obstacles to consistent condom use within couples who are aware of their HIV-serodiscordant status have been inadequately examined in China.

Accordingly, we conducted a study among marriage license applicants in a rural area of China, where HIV spread among former commercial plasma donors. In this report, we first describe the patterns of HIV-related knowledge, perceived vulnerability to HIV infection, HIV test result disclosure, and risk-taking behaviors among the applicants. We also examine the factors associated with anticipated consistent condom use. An understanding of common risky sexual behaviors will provide a basis for developing effective intervention programs targeted to eliminate unsafe sexual contact within couples and to reduce HIV mother-to-child transmission.

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Materials and Methods

Study Site

This study was conducted in a rural county in Anhui Province. Anhui is located in Eastern China, where 83% of the population is composed of rural residents. The province is facing a major public health crisis because of the increasing spread of HIV/AIDS. The first AIDS case in Anhui was reported in December 1994. From 1994 to 2004, 2068 HIV cases have been reported from 16 cities and 54 counties in the province, which ranks seventh among 31 Chinese provinces.13 The infection rate continues to accelerate in Anhui with 401 cases reported in 2002 and 967 cases in 2003, reflecting a 2.4-fold increase. The majority of HIV cases were among farmers (95.3%) and former plasma blood donors (85.8%). The county evaluated in this study is located in the north of Anhui Province, in the center of the HIV epidemic, and has a population of 1.4 million. In the county under study, approximately 94% of the population lives in rural areas (villages) and the remainder live in the county town. A typical county in rural China consists of a county town where the county administration agencies and small factories are located and villages where farmers live. By 2003, 372 HIV cases had been reported (147 in 2002, 164 in 2003). Similar to the province as a whole, most of the infected cases (85%) were among former plasma donors.

The study was conducted at the Center for Certificate Issue where marriage licenses are issued by the County Department of Civil Affairs. All applicants from both rural and urban areas in the county are required to apply for a marriage license at the center. The study protocol received approval from the Institutional Review Boards at Wayne State University in the United States and at Anhui Medical University in China.

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Study Population

A baseline feasibility study for HIV counseling among rural couples applying for a marriage license was conducted in October and November 2003. Only the license applicants from rural villages were included in the study; rural residence was determined by identification card. The first 5 rural couples applying in the morning and the first 5 rural couples applying in the afternoon were invited to participate until the sample size was achieved. An average of 15 to 20 couples from both rural villages and the county town applied for a certificate each day. The China Marriage Law requires both partners of a couple to be present at the center at the time of application. The study participants provided with informed consent and were presented with a small gift as a stipend for their participation.

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Interview

An anonymous questionnaire was administered to the subjects. The research team and the local public health staff members reviewed each question on the questionnaire to ensure the appropriateness of the questions. Some changes on questions were made accordingly. An interview was administered in a separate room for each partner. Trained interviewers were paired with respondents of the same gender. There were 2 parts to the questionnaire. The first part was delivered face-to-face and included less sensitive questions such as sociodemographic characteristics, issues related to dating and marriage, and knowledge of and attitudes about HIV/AIDS. The second part of the interview included questions regarding sexual behavior and was administered using a tape recorder and earphones.14 All questions and response options were prerecorded on tapes. The participants used earphones to listen to the questions and mark their responses on a coded answer sheet that did not contain the questions or any identifying information. Observers including the same-gender interviewer were not allowed in the interview room during the second part.

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Measurement

HIV Knowledge.

Knowledge regarding transmission and prevention of HIV/AIDS was measured by 13 true/false (unsure) questions. One point was given for a correct answer, with a possible score ranging from 0 to 13 points.

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Perceived Vulnerability to HIV Infection.

Perceived vulnerability was measured by the following questions: 1) “People have different ideas about their risk of getting HIV/AIDS. What do you think the chances are that you will acquire HIV?” and 2) “What do you think the chances are that your spouse will acquire HIV?” Response choices were: (1) likely, (2) unlikely, or (3) unsure.

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Sexual Behaviors.

Sexual behaviors were assessed by questions regarding 1) premarital sex (yes/no); 2) multiple sex partners (yes/no), defined as having had more than 1 sexual partners; and 3) condom use with multiple sex partners (often or always/sometimes/never used).

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Condom Use.

Two questions were used to measure condom use and anticipation of condom use. Among subjects who had multiple sexual partners, the frequency of condom use with sexual partners other than his or her spouse was asked (often, always, sometimes, or never). All participants were asked: “If you or your spouse were infected by HIV, would you use condoms consistently when you have sex with your spouse?” (yes, not, or unsure).

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Analysis

Two research assistants independently entered the data into a computerized database using Epi-Info 6.12 (Centers for Disease Control and Prevention, Atlanta, GA). Associations between 2 categorical variables were examined using chi-squared tests, whereas t tests were used for a continuous outcome. Multiple logistic regression analysis, using SAS 8.02 (SAS Institute, Cary, NC), was performed to estimate adjusted odds ratios (aOR) and their 95% confidence intervals (CIs) of factors associated with the anticipation of condom use.

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Results

Description of the Study Population

During the study period, 850 applicants (425 couples) from rural areas applied for a marriage certificate in the center. Among them, 632 (316 couples) were invited to participate in the study. Twenty-seven (4.3%, 27 of 632) refused to participate. Thus, 605 (302.5 couples, 1 male missing) applicants were interviewed. The mean age of the respondents was 23.8 (standard deviation [SD], 2.5) years, 23.3 (SD, 2.4) years for females and 24.5 (SD, 2.5) years for males. The majority had completed at least a middle school education (61.2%), had an agricultural job (66.8%), and had a history of rural-to-city migration (66%) (Table 1).

TABLE 1

TABLE 1

Approximately half of the subjects (56.5%) reported that they had been introduced to their spouse by matchmakers (Table 1). The mean interval from dating to marrying was 2.1 years (SD, 1.5). More males (64.6%) than females (36%) reported that they knew their fiancé or fiancée very well (chi-squared = 54.2, P <0.01). More than half (62%) of the subjects planned to try to become pregnant within 1 year; 7% did not intend to have a baby.

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Sexual Behavior and Condom Use

More males (64.6%) than females (52.1%) reported having had premarital sex (chi-squared = 9.6, P <0.01) and multiple sex partners (12.6% and 6.9%, respectively, chi-squared = 5.5, P = 0.02). Eighty-five percent of the subjects who had engaged in premarital sex had such sex with their intended spouse. Among those who had multiple sexual partners, 8.5% reported often or always using condoms with sexual partners rather than their spouse (9.5% for females, 7.9% for males). Two percent of sexually experienced subjects (7 of 353) reported having had a sexually transmitted disease. Fourteen subjects (2.3%) reported having sold their blood.

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HIV Knowledge, Perceptions, and Attitudes Toward HIV Infection

The mean score of HIV knowledge was 5.61 (SD, 3.84), 5.46 (SD, 3.71) for females and 5.76 (SD, 3.96) for males (t = 0.96, P = 0.34) (Table 2). At the couple level, 28.2% of the couples (85 of 302) had a score greater or equal to the mean level (5.61). A small proportion of the subjects perceived themselves to be vulnerable (13.4%) and their spouses to be vulnerable (6.4%) to HIV infection. More males (65.9%) than females (51.8%) would plan not to have a baby if they were to learn that 1 of them was HIV-positive (chi-squared = 7.6, P <0.01). However, only 36.8% of the couples (111 of 302) agreed that they would avoid a pregnancy. Thirty-nice percent of the couples (119 of 302) knew that HIV could be transmitted within HIV-discordant couples, and 41% (125 of 302) knew that HIV could be vertically transmitted from parents to a child. Only 2 couples realized that anti-HIV drugs were available to prevent vertical transmission.

TABLE 2

TABLE 2

Of the subjects, 40% agreed with the statement that consistent use of condoms could prevent HIV infection. Fifty-four percent of females and 68.5% of males would use condoms consistently if they or their spouse acquired HIV (chi-squared = 11.9, P <0.01) (Table 2). At the couple level, 42.7% (129 of 302 couples) of the couples agreed that they would use condoms consistently if 1 of them were HIV-positive.

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Disclosure of HIV Testing Result and Its Anticipated Consequences

Sixty-four percent of the subjects were willing to accept HIV testing, although for only 43.7% (132 of 302) of the couples did both members indicate willingness to accept the testing. Approximately 75% of the subjects were willing to disclose positive results to their spouses, 62.3% to their parents, 56.9% to their brothers or sisters, and 31.6% to their friends. The anticipated consequences resulting from disclosure included being stigmatized by their spouse (20.5%), breakup of the marriage (31.7%), physically abused by their spouse (22%), and disowned by the family (27.9%) (Table 3).

TABLE 3

TABLE 3

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Factors Associated With Anticipation of Condom Use

We compared the group reporting that they would use condoms consistently when having sex with their spouse with the group not reporting the acceptance of condom use when 1 member of the couple acquired HIV infection (Table 4). The multivariate analysis indicated that those who received a high school education or above, who felt that they knew their fiancé or fiancée very well, had greater HIV knowledge, did not plan to have a baby if a spouse was infected, realized that an HIV-infected spouse could transmit HIV to their baby, or had premarital sex were more likely to accept condom use. Acceptance was also positively associated with age.

TABLE 4

TABLE 4

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Discussion

This study, conducted in an area with a relatively high HIV prevalence, examined HIV-related risks among rural marriage applicants and the potential for HIV transmission between husbands and wives and from parents to children in China. The findings clearly demonstrate that HIV-related risks exist among the marriage license applicants, and there is a potential that HIV could be transmitted both to spouses and children.

In a number of provinces, mostly in central China, HIV infection through illegal plasma-collection practices constitutes a major important high-risk activity.5,15,16 The role of unsafe plasma donation practices was recognized more than 9 years ago.5 Given the fact that HIV has been spreading in the area for several years, it is alarming and disappointing to learn from the current study that couples planning to marry have a low level of HIV knowledge and perception of personal vulnerability to HIV infection. We compared the results from the current study with those from our previous study conducted 6 years ago in the same area. HIV knowledge and awareness have not improved significantly since then.17 Because people with low HIV knowledge and low perceived vulnerability to HIV infection are less likely to take action to protect themselves and their families from HIV infection,18 it is essential to increase awareness in the rural areas as the first step to curb the epidemic. The China AIDS Action Plan (2001–2005) has set a goal that 45% of rural residents and 80% of the population at risk should understand the ways to prevent the transmission of HIV by the end of 2005. To accomplish the goal, China needs to increase intervention efforts, especially in rural China, where the majority of HIV-infected persons reside.

In the past 2 decades, China has experienced dramatic social changes associated with rapid economic growth and reform.19 Traditional attitudes toward sex, marriage, and family have changed.20,21 More and more young people are practicing premarital sex. As cited by Watts,22 a recent survey by the China Family Planning Agency found almost 70% of men and women were not virgins when they married, up from 16% at the end of the 1980s. In urban areas, 9 of every 10 people who sign the marriage registry had a previous sexual experience.22 Similarly, according to a systematic review, from 54% to 82% of unmarried women in China have had sexual experience.21 In this study, we found that 58% of the subjects reported having had premarital sex and 9.7% reported having had more than 1 sexual partner. The percentage of multiple partners reported in this study is different from the one reported by Parish and colleagues (19% for men and 5% for women)23 and by Liu and colleagues (6% of rural residents).24 The difference may have resulted from including different populations. A national stratified probability sample of individuals was interviewed in Parish’s study, and Liu and colleagues conducted their study 14 years ago (1989–1990). Most of the individuals having had multiple sexual partners did not use condoms, although the proportion of the subjects reporting multiple sexual partners was relatively small compared with other developing countries.2

In 1997, we conducted a study in China to examine individual acceptance of voluntary HIV testing and the scope of test result disclosure.25,26 The reported acceptance rate was 54% (575 of 1057) among the total study population and 88% (575 of 653) for those who had ever heard of HIV/AIDS. In the current study, the percentage was 64%. Seventy-five percent of subjects would disclose their HIV-positive result to their spouses, although they anticipated that they might be stigmatized, physically abused, or disowned by their spouse or family. The high proportion of disclosure might result from the fact that the acquisition of HIV infection in the area was through commercial blood donation. Compared with the other 2 stigmatized behaviors, casual sexual contacts and shearing drug needles, commercial blood donation practice was socially acceptable in rural areas. This highlights the value of voluntary counseling and testing services (VCT) for couples, which can increase HIV awareness, assist partners in discussing sex, and reduce risk. Studies have confirmed the success of voluntary counseling and testing programs for reduction of unprotected intercourse and increased condom use among HIV-serodiscordant couples.27 Stigma, however, remains a problem that needs to be resolved.

Although studies have found that the consistent use of condoms by serodiscordant heterosexual couples reduces the transmission of HIV by 87%,28 condom use among married couples is low worldwide.29 Prevention of HIV transmission among married couples is, therefore, a particularly difficult public health challenge. A recent report showed that 73% of study participants with a serodiscordant partner reported consistent condom use.30 Another study found that only 39% of serodiscordant heterosexual couples reported that they had always used condoms in the past 6 months, despite awareness of their HIV-serodiscordant status.31 The finding that 61% of individuals and only 42.7% of couples would use condoms if 1 of them was infected highlights the challenge to halt HIV transmission at the family level and demonstrates an urgent need for risk-reduction intervention for couples.

A variety of psychosocial factors affect couples’ decision to consistently use condoms. Our finding that 23% of females and 8.6% of males desire children in the future, even after learning that they or their partner is HIV-positive, and the low rate of intended condom use underscores the magnitude of the potential risk. Chen and colleagues reported that 28% of HIV-positive men and 29% of HIV-positive women receiving medical care in the United States desired children.32 Another study conducted among urban Rwandan women showed that the 2-year incidence of pregnancy was 43% in HIV-positive and 58% in HIV-negative women after HIV testing and counseling, and neither condom use nor spermicide use was associated with a lower incidence of pregnancy in either serostatus group.33 Chinese culture and the Confucian doctrine of filial piety support the desire for large families. Although China promotes the 1-child policy, the policy has not been strictly implemented in the rural areas. Families with 2 or more children are common in rural villages. This cultural perspective presents a substantial obstacle to facilitating condom use among couples of reproductive age, especially when individuals have a sense of low perceived susceptibility.34 This finding indicates that behavioral intervention programs should provide more options for HIV-positive subjects beyond condom use, for example, the inclusion of antiretroviral therapy. However, few of the couples were aware that vertical transmission could be prevented. Thailand’s successful national program for preventing mother-to-child HIV transmission provides a good model for China in this regard.35,36 In addition, we found that individuals who felt they knew their fiancés or fiancées very well before marriage were more likely to anticipate condom use if their spouse acquired HIV infection. This finding may suggest that a good courtship can generate responsibility in couples to protect spouses from HIV infection.

Several limitations to this study need to be noted. HIV-related risky sexual behaviors are not socially accepted in rural China; thus, it is possible that study participants may have provided socially desirable responses and failed to report multiple sexual partners and unprotected sex. However, the use of the tape recorder technique with a 2-part questionnaire, developed by Liu and Detels14 to ask sensitive questions, may maximize the accuracy of responses. It has been used to inquire about sensitive behaviors in China,17,37,38 Vietnam,39 Indonesia,40 and Thailand.41 The single study site may limit generalizability of our findings. Responses to the questions on consistent condom use, testing result disclosure, and its anticipated consequences were based on personal perception and were hypothetical and may not reflect actual practices. Lastly, because most of the responses were measured retrospectively, recall bias may be present.

Despite these limitations, our study provides valuable information on HIV-related risks among young rural residents in China. The findings suggest that more rigorous intervention measures need to be implemented in rural areas, targeting an increase of HIV-related knowledge about and awareness of personal vulnerability to HIV infection and reduction of HIV-related stigma. HIV VCT programs have been widely implemented in developing countries. However, acceptability is related to the local culture and social norms, which may need to be modified through intervention programs. Successful reduction of the HIV epidemic in Thailand and Cambodia demonstrates that the epidemic can be halted in developing countries despite poor resources. China needs to learn from these 2 countries about the strategies that are effective. Our study underscores the need for national programs to prevent HIV infection within couples, especially in rural areas.

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