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Volume 331:341-346 August 11, 1994 Number 6 Next

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ABSTRACT

Background Worldwide, the predominant mode of human immunodeficiency virus (HIV) transmission is heterosexual intercourse, but the risk of heterosexual transmission and the effectiveness of measures to prevent it are not well defined.

Methods We conducted a prospective study of HIV-negative subjects whose only risk of HIV infection was a stable heterosexual relationship with an HIV-infected partner. Every six months the subjects were interviewed, tested for HIV, and counseled about safe sexual practices.

Results A total of 304 HIV-negative subjects (196 women and 108 men) were followed for an average of 20 months. During the study, 130 couples (42.8 percent) ended their sexual relationships, most often because of the HIV-infected partner's illness or death. Of the 256 couples who continued to have sexual relations for more than three months after enrollment in the study, only 124 (48.4 percent) used condoms consistently for vaginal and anal intercourse. Among these couples, none of the seronegative partners became infected with HIV, despite a total of about 15,000 episodes of intercourse. Among the 121 couples who used condoms inconsistently, the rate of seroconversion was 4.8 per 100 person-years (95 percent confidence interval, 2.5 to 8.4). Eleven couples refused to answer questions about condom use. The risk of transmission increased with advanced stages of HIV infection in the index partners (P<0.02) and with genital infection in the HIV-negative partners (P<0.04). Withdrawal to avoid ejaculation in the vagina had a protective effect in uninfected women (P<0.02).

Conclusions Consistent use of condoms for heterosexual intercourse is highly effective in preventing the transmission of HIV. Among couples not using condoms regularly, the risk of HIV transmission varies widely. .

Although the use of condoms is still the only available method to prevent HIV infection in people who have sexual contact with HIV-infected partners, the effectiveness of condoms in preventing infection is not known with precision⁵. The incidence of condom breakage during vaginal intercourse has been estimated at around 1 percent,⁶ but most cases of sexual transmission among couples using condoms are related to inconsistent use of condoms rather than to failure of the barrier method itself⁵.

A cross-sectional analysis of data from a multicenter European study examined the risk factors for both male-to-female and female-to-male transmission of HIV⁷. We present here the prospective component of that study, which includes follow-up data on couples in which one partner was HIV-positive and the other was HIV-negative. The aims of the longitudinal study were to determine the rate of condom use after counseling, the effectiveness of condoms in preventing HIV transmission, and the rate of and risk factors for transmission among couples who did not use condoms consistently.

Methods

Between March 1987 and March 1991, HIV-infected men and women (index partners) and their heterosexual partners were recruited in hospital wards, outpatient clinics, clinics for the treatment of sexually transmitted diseases, and local public health departments (HIV-screening centers and drug-treatment centers). The study excluded occasional partners and partners with other risk factors for HIV infection (intravenous drug use, male homosexual relations, receipt of unscreened blood products, sexual contact with multiple partners, or one or more heterosexual partners who were from sub-Saharan Africa or had one of the above risk factors). Study participants were interviewed with the use of a standardized questionnaire translated from English into the language used at the participating center. The index partners underwent HIV testing at the time of enrollment in the study, and their HIV-seronegative partners were seen every six months, until June 1992. A total of 378 couples recruited at 10 centers in eight countries of the European Community were eligible for the prospective study.

At each visit, the couples were counseled about the risk of HIV infection and about safe sexual practices, according to the policies at the center. At follow-up visits, to avoid any influence of knowledge of the HIV-test results on the reporting of sexual behavior, the partners were interviewed before being told the results. For each follow-up period, the subjects were asked about their history of risk factors for HIV infection, the number of sexual partners, contraceptive practices, use of condoms, and sexual practices. A history of sexually transmitted diseases was also obtained.

HIV serologic status was determined by the enzyme-linked immunosorbent assay and confirmed by Western blotting or radioimmunoprecipitation in the laboratories of the participating centers. Information on the index partners' clinical status, according to the classification of the Centers for Disease Control and Prevention (CDC),⁸ and lymphocyte counts per cubic millimeter was obtained from medical records.

Partners seen at least twice (at enrollment and at least one follow-up visit) were included in the study. The duration of exposure to HIV was defined as the time from enrollment in the study to the last negative HIV test, for subjects who remained uninfected and still had sexual contact with their infected partners in June 1992; the time to the last sexual contact, for subjects who remained uninfected but ceased sexual relations with their infected partners; or the midpoint between the last negative test and the first positive test, for subjects who seroconverted. The frequency of condom use during follow-up was estimated as the mean of the frequencies reported during the follow-up visits.

Factors linked to loss of follow-up, cessation of sexual contact, and frequency of condom use were analyzed with Fisher's exact test and the chi-square test for categorical variables and with Student's t-test for continuous variables. Multivariate analyses were computed by logistic regression. Calculation of the 95 percent confidence intervals for rates of seroconversion according to person-years was based on the Poisson distribution. Risk factors for seroconversion were analyzed among the subsample of couples who had unprotected sexual contact during the study, with the use of the actuarial life-table method, and survival curves were compared with the use of the Breslow test⁹.

Results

Of the 378 eligible couples, 256 (67.7 percent) continued to have sexual relations (93 with female index partners and 163 with male index partners), 48 (12.7 percent) ceased having sexual relations within three months after their first visit, and 74 (19.6 percent) were lost to follow-up. The proportion of couples lost to follow-up was not significantly associated with the center (range, 5 to 31 percent) or with any of the sexual, demographic, or medical characteristics documented at the time of enrollment (Table 1).

View this table: [in this window] [in a new window]   Table 1. Couples Lost to Follow-up, According to Characteristics at the Time of Enrollment in the Study.

 
Continuation of Sexual Relations

A total of 130 couples (42.8 percent) ceased having sexual relations during the study period. Forty-eight couples stopped having sexual contact within three months after enrollment, and 82 couples did so later during the follow-up period. In nearly one third of these couples (40 of 130), the index partners had died. In 19 of the remaining 90 couples (21.1 percent), the index partners had AIDS. In comparison, the index partners had AIDS in only 18 of the 174 couples (10.3 percent) who continued to have sexual relations (P<0.02). Among the couples with asymptomatic index partners, the initially uninfected partners tended to be younger in the couples who continued to have sexual relations than in the couples who did not (median age, 28 vs. 30 years; P<0.05). The couples continuing to have sexual relations also had more frequent sexual contact before the positive HIV test of the index partner (median number of contacts per week, three vs. two; P<0.01) and were more likely to use condoms after the positive test (92 percent vs. 77 percent; P<0.05). The continuation of sexual relations was not associated with the sex of the index partner, the mode of infection in the index partner, or the previous duration of the relationship.

Subsequent analyses concern the 256 couples who continued to have sexual contact for more than three months after enrollment in the study. The median duration of exposure to infection for the 256 uninfected partners was 22 months.

Frequency of Condom Use

The 256 couples were classified according to the frequency of condom use during follow-up. Only 124 couples (48.4 percent) used condoms for every episode of vaginal or anal intercourse (consistent condom users); 121 couples (47.3 percent) did not always use condoms (inconsistent condom users). Among the 121 couples who were inconsistent users, 61 (50.4 percent) used condoms for at least half their sexual contacts but not for every contact, and 60 (49.6 percent) rarely or never used condoms. Eleven of the 256 couples (4.3 percent) refused to answer questions about their sexual behavior, although the uninfected partners agreed to follow-up serologic testing.

In the univariate analysis (Table 2), consistent condom use was not associated with the age or sex of the index partner or with the duration of follow-up. The median duration of the relationship before enrollment in the study was longer among the consistent users than among the inconsistent users (36 vs. 24 months, P<0.01). Consistent use of condoms was more frequent among couples in which the index partner had received a diagnosis of AIDS before enrollment in the study (70.8 percent vs. 48.4 percent, P<0.04). The proportion of consistent condom users varied according to the mode of infection in the index partner, ranging from 40.1 percent for infection through drug use to 73.2 percent for infection through sexual contact. The proportion of consistent condom users varied according to the enrolling center (range, 18 to 79 percent). To take into account the associations among these variables, all were included in a logistic-regression model. After adjustment for the center, the mode of infection in the index partner (P<0.001), the clinical status of the index partner at the time of enrollment (P<0.05), and the duration of the relationship before enrollment (P<0.04) were independently associated with consistent condom use.

View this table: [in this window] [in a new window]   Table 2. Rate of Consistent Condom Use, According to the Characteristics of the Index Partner, the Duration of the Relationship, and the Duration of Follow-up.

 
The other modifications in sexual behavior recorded during the study included a decreasing frequency of sexual contacts and the cessation of anal sex, sex during menses, and oral sex. Throughout the study, the consistent condom users reported a lower frequency of sexual contacts and lower frequencies of oral and anal sex and sex during menses than did the inconsistent users (Figure 1).

View larger version (27K): [in this window] [in a new window]   Figure 1. Sexual Practices among 124 Couples Using Condoms Consistently (Solid Bars) and 121 Couples Using Condoms Inconsistently (Open Bars). The distinction between consistent and inconsistent condom use pertains to use during the study period (after enrollment). The proportions and frequencies shown refer to engagement in the particular sexual practice at least once during each of three periods: before the first positive test for HIV in the index partner, among couples who had already had sexual relations at that time (194 of 245 couples); at the time of enrollment in the study; and during follow-up.

 
Seroconversion Rates

Seroconversion occurred in 12 of the 256 partners followed (8 women and 4 men), for a seroconversion rate of 2.3 per 100 person-years (95 percent confidence interval, 1.2 to 4.0) for the whole group.

No seroconversion occurred among the 124 couples who used condoms for each vaginal or anal contact (95 percent confidence interval, 0 to 1.5 per 100 personyears). These 124 couples had approximately 15,000 protected sexual contacts during the study. Among these couples, 49 (39.5 percent) continued to practice fellatio, and 39 of the 49 did so without the use of condoms. The 95 percent confidence interval for the null rate of seroconversion through unprotected fellatio was 0 to 4.7 per 100 person-years.

No seroconversion occurred among the 11 couples who did not provide information on condom use.

Risk Factors for Seroconversion among Inconsistent Condom Users

Twelve initially uninfected partners seroconverted among the 121 couples using condoms inconsistently for vaginal or anal sex, corresponding to a seroconversion rate of 4.8 per 100 person-years (95 percent confidence interval, 2.5 to 8.4).

Since none of the seroconversions occurred after 24 months of exposure, the estimated cumulative incidence of seroconversion at 24 months is presented here. However, the statistical test relies on a global comparison of the survival curves. The estimated cumulative incidence of seroconversion at 24 months among the 121 inconsistent condom users was 12.7 percent (95 percent confidence interval, 5.9 to 19.5). In the univariate analysis (Table 3), the cumulative incidence of seroconversion did not differ significantly between the female and male index partners (11.4 and 13.4 percent, respectively).

View this table: [in this window] [in a new window]   Table 3. Cumulative Rate of Seroconversion at 24 Months among the 121 Couples Not Consistently Using Condoms.

 
The cumulative incidence of seroconversion differed significantly according to the clinical status of the index partner (P<0.02). Among couples in which the index partner was in an advanced stage of infection at the time of enrollment in the study (stage IV in the CDC classification or a CD4 cell count below 200 per cubic millimeter), the cumulative incidence of seroconversion in the uninfected partner was 48.7 percent, as compared with 7.8 percent among the couples in which the index partner remained asymptomatic and had a CD4 count above 199 per cubic millimeter throughout the follow-up period. Among couples in which the infection in the index partner progressed from an asymptomatic stage at the time of enrollment (with a CD4 count >199 per cubic millimeter) to an advanced stage during follow-up, the estimated cumulative incidence of seroconversion in the uninfected partner was 11.7 percent.

Five nonindex partners reported ulcerative genital infections during follow-up, and nine nonindex partners reported nonulcerative infections. Three of the 12 partners who seroconverted had genital infections: 1 had balanitis, 1 a recurrence of herpes, and 1 syphilis (a woman whose HIV-infected partner had acquired syphilis from someone not included in the study). The cumulative incidence of seroconversion was significantly lower (P<0.04) among partners reporting no genital infections (12.8 percent) than among those reporting nonulcerative infections (33.3 percent) or ulcerative infections (40.0 percent).

Among the eight women who continued to have unprotected anal sex with their HIV-infected male partners, the cumulative incidence of seroconversion was 27.8 percent, as compared with 11.7 percent among the women not reporting such practices (P>0.15). The frequency of sexual contacts (median, two per week), the use of oral contraceptives, and the practice of oral sex and sex during menses were not associated with the risk of seroconversion. The couples using condoms for at least half but not all sexual contacts had about the same risk of seroconversion as the couples not using condoms (10.3 and 15.0 percent, respectively; P>0.60). On the other hand, withdrawal before ejaculation was associated with a lower risk of male-to-female transmission of HIV (P<0.02). The cumulative incidence of seroconversion was 0 percent among the couples who nearly always practiced withdrawal before ejaculation, 7.2 percent among those who did so about half the time, and 32.4 percent among those who rarely or never did so.

The number of subjects who seroconverted was too small to allow a multivariate analysis.

Discussion

It is reassuring that no HIV transmission occurred among the couples reporting consistent use of condoms. However, only half the couples who continued having sexual relations used condoms consistently. Since the counseling was not standardized, it is difficult to relate it to these results. Condoms were reported to have a low level of acceptability among drug users and their non-drug-using partners in New York,¹⁰ but not in a cohort of couples in California².

There is still much debate about whether unprotected oral sex should be considered a safe sexual practice¹¹. People with no risk factors for HIV infection other than unprotected oral sex with an infected partner represent an ideal population for the estimation of the risk of transmission by this practice. In our study, no seroconversion occurred in the small subsample of 39 partners who had unprotected oral sex while consistently using condoms during vaginal intercourse. The 95 percent confidence interval for this null rate of transmission is 0 to 4.7 per 100 person-years, representing a risk that, although significantly lower than the risk associated with unprotected vaginal intercourse, cannot be assumed to be negligible.

Attempts have been made to estimate the risk of transmission per episode of vaginal intercourse^12,13. Our data, which are prospective rather than retrospective, allow a more reliable estimation of that risk, and the results of our analyses confirm that the risk is not constant from one contact to another. For example, among the 121 couples who used condoms inconsistently during an estimated 12,000 unprotected sexual contacts, the rate of transmission per contact was 1 per 1000 (95 percent confidence interval, 0.5 to 1.7). When the risk was estimated according to the stage of HIV infection in the index partner, the rate of transmission per contact was 5 per 1000 (95 percent confidence interval, 1.4 to 13.1) if the index partner was in an advanced stage of infection and 0.7 per 1000 (95 percent confidence interval, 0.3 to 1.4) if the index partner was asymptomatic. Thus, the clinical status of the HIV-infected partner greatly influences the risk of transmission per sexual contact, suggesting that some people are highly infectious and others hardly infectious at all. Repeated acts of unprotected sexual intercourse are not independent of one another. For example, if someone has had 100 sexual contacts with a partner who has a very low level of infectivity, the risk of transmission is low. However, if someone has sex with 100 different infected partners, there is a high probability that at least one of the partners is highly infectious.

The identification of risk factors for HIV is limited in the present analysis because of the small number of partners who seroconverted. Consequently, the power of the tests is low, and nonsignificant differences should be interpreted with caution. In particular, although no difference was found between the risk of male-to-female transmission and that of female-to-male transmission, one should not conclude that the risk of transmission is similar in both directions. Indeed, recent studies^7,14 suggest that male-to-female transmission is twice as efficient as female-to-male transmission. Anal sex does not significantly increase the risk of transmission to the female partner¹⁵. This result could be due to a lack of power, since only eight women continued to have unprotected anal sex with their HIV-infected partners; the cumulative incidence of seroconversion among these women was 27.8 percent, as compared with 11.7 percent among the women who did not have unprotected anal sex.

Consistent withdrawal before ejaculation appears to provide female partners with some protection against HIV infection. The avoidance of contact between the infected sperm and the cervicovaginal mucosa, either by the use of condoms or by withdrawal before ejaculation, may provide a higher level of protection than that provided by inconsistent condom use alone. However, pre-ejaculatory fluid may be a vector for the transmission of HIV¹⁶. Moreover, withdrawal is less effective than condom use as a contraceptive measure (efficacy, 82 percent vs. 88 percent),¹⁷ and the potential protection is only against male-to-female transmission. Withdrawal as a method of protection relies solely on the action of the infected male partner, with no possibility of control by the female partner, and unlike condom use, withdrawal does not provide protection from other sexually transmitted diseases, which may be cofactors for the transmission of HIV¹.

Despite the low power of this study, the data indicate that the stage of HIV infection in the index partner is a strong risk factor for transmission, confirming the results of previous studies^7,18. Therefore, the variation in transmission rates among studies in different countries may be due, at least in part, to differences in the stage of the HIV epidemic and in the proportions of patients with advanced infection. In our study, there were too few index partners with an advanced stage of HIV infection to permit assessment of the potential protective effect of anti-HIV therapy¹⁸.

The results of our study add support to the view that genital infections, especially those that are ulcerative, facilitate the transmission of HIV¹. Most of the genital infections in our subjects were caused by herpesvirus or candida. These infections occurred among consistent condom users as well as inconsistent users and thus may not have been acquired sexually during the study period. Since a genital examination was not performed systematically at each study visit, we cannot exclude the possibility that some genital infections were missed, but it is likely that the missed episodes were equally distributed among the subjects who seroconverted and those who did not, since the interviews were conducted before the subjects knew the HIV-test results.

Finally, it should be stressed that nearly half the couples (130 of 304) had stopped having sexual relations by the time the study ended, perhaps to protect themselves against the transmission of HIV. This phenomenon, together with the ethical requirements for counseling, limits what can be learned from longitudinal studies of sexual transmission between partners. It may be useful to examine the immunologic and virologic characteristics of the few couples who remain discordant for HIV infection despite high risks of transmission. The effectiveness of other preventive methods, including local microbicides, deserves further study in large populations at risk of acquiring HIV infection through sexual contact.

Supported by grants from the Commission of the European Communities.

We are indebted to M. Laga and A. Downs for their participation and advice.

Source Information

The members of the European Study Group on Heterosexual Transmission of HIV are listed in the Appendix.

From the European Centre for the Epidemiological Monitoring of AIDS, Hopital National de Saint-Maurice, 14 rue du Val d'Osne, 94410 Saint-Maurice, France, where reprint requests should be addressed to Dr. de Vincenzi.

References

1. Laga M, Manoka A, Kivuvu M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS 1993;7:95-102. [Medline]
2. Padian NS, O'Brien TR, Chang Y, Glass S, Francis DP. Prevention of heterosexual transmission of human immunodeficiency virus through couple counseling. J Acquir Immune Defic Syndr 1993;6:1043-1048.
3. Kamenga M, Ryder RW, Jingu M, et al. Evidence of marked sexual behavior change associated with low HIV-1 seroconversion in 149 married couples with discordant HIV-1 serostatus: experience at an HIV counselling center in Zaire. AIDS 1991;5:61-67. [Medline]
4. Saracco A, Musicco M, Nicolosi A, et al. Man-to-woman sexual transmission of HIV: longitudinal study of 343 steady partners of infected men. J Acquir Immune Defic Syndr 1993;6:497-502.
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6. Chan-Chee C, De Vincenzi I, Sole-Pla MA, Ancelle-Park R, Brunet JB. Use and misuse of condoms. Genitourin Med 1991;67:173-173. 
7. European Study Group on Heterosexual Transmission of HIV. Comparison of female to male and male to female transmission of HIV in 563 stable couples. BMJ 1992;304:809-813.
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12. Kaplan EH. Modeling HIV infectivity: must sex acts be counted? J Acquir Immune Defic Syndr 1990;3:55-61.
13. Wiley JA, Herschkorn SJ, Padian NS. Heterogeneity in the probability of HIV transmission per sexual contact: the case of male-to-female transmission in penile-vaginal intercourse. Stat Med 1989;8:93-102. [Medline]
14. Haverkos HW, Battjes RJ. Female-to-male transmission of HIV. JAMA 1992;268:1855-1857.
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The European Study Group on Heterosexual Transmission of HIV includes the following centers and investigators: the European Centre for the Epidemiological Monitoring of AIDS, Hopital National de Saint-Maurice, Saint-Maurice, France (coordinating center): I. de Vincenzi, R.A. Ancelle-Park, and J.-B. Brunet; Istituto Malattie Infettive, Universita di Bologna, Bologna, Italy: P. Costigliola, E. Ricchi, and F. Chiodo; Athens School of Hygiene, Athens, Greece: A. Roumeliotou and G. Papaevangelou; Sozialpadagogisches Institut, Berlin, Germany: M. Kraus and W. Heckmann; Department of Public Health and Environment, Municipal Health Service, Amsterdam: R.A. Coutinho and H.J.A. van Haastrecht; Programa del SIDA, Generalitat de Catalunya, Barcelona, Spain: J. Casabona and J. Tor; Infectious Diseases Service, Health Institute Carlos III, Madrid: J. Gonzalez-Lahoz and R. Andres-Medina; Institute of Tropical Medicine, Antwerp, Belgium: M. Vandenbruaene and J. Goeman; Immunopathologie Clinique, Hopital H. Mondor, Creteil, France: A. Sobel; and Infectious Disease Unit, City Hospital, Edinburgh, United Kingdom: R. Brettle and R. Robertson.

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