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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e3181a396eb
Articles

A Systematic Review of Epidemiologic Studies Assessing Condom Use and Risk of Syphilis

Koss, Catherine A. BS*†; Dunne, Eileen F. MD, MPH*; Warner, Lee PHD, MPH‡

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From the *Division of STD Prevention, National Center for HIV, Viral Hepatitis, STD, and TB Prevention, and †The CDC Experience Applied Epidemiology Fellowship, Centers for Disease Control and Prevention, Atlanta, Georgia; and ‡Division of Reproductive Health, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia.

The authors thank Dr. Robert Johnson, Dr. Lauri Markowitz, Dr. Stuart Berman, Dr. Emilia Koumans, and Dr. Thomas Peterman for carefully reviewing this manuscript.

The findings and conclusions of this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Correspondence: Eileen F. Dunne, MD, MPH, Division of STD Prevention, Centers for Disease Control and Prevention, 1600 Clifton Rd. MS E-02, Atlanta, GA 30333. E-mail: edunne@cdc.gov.

Received for publication August 12, 2006, and accepted February 3, 2009.

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Abstract

Background: Although systematic reviews of epidemiologic studies have been conducted for condom use and the risk of several sexually transmitted diseases, there have been no such reviews for condom use and syphilis.

Methods: A systematic literature review of epidemiologic studies published from 1972 to 2008 was conducted to evaluate study methods and measures of association reported for condom use and risk of syphilis.

Results: All 12 included studies had significant methodologic limitations. Nine (75%) studies were cross-sectional. Although 11 (92%) studies assessed consistent condom use, no studies assessed correct use or condom use problems, nor did any document exposure to a partner infected with syphilis. Ten studies had insufficient information to distinguish prevalent from incident infections. Two studies that assessed both incident infection and consistent condom use suggested a reduced risk of syphilis with consistent condom use; 1 study was statistically significant.

Conclusions: Significant methodologic limitations exist for all reviewed studies of syphilis and condom use. Among the 2 most rigorously designed studies, both suggested a reduced risk of syphilis with consistent condom use. Additional studies incorporating rigorous methods are needed to further assess the effect of condom use on risk of syphilis.

The number of reported syphilis cases in the United States has steadily increased since declining in 2000 to the lowest levels ever reported.1 In 2006, nearly 10,000 primary and secondary (P&S) syphilis cases were reported, an 11.8% increase from the previous year. Most of these cases occurred among men, with men who have sex with men (MSM) accounting for 64% of all primary and secondary (P&S) cases, although rates have also increased among women. Syphilis disproportionately affects blacks (43.2% of P&S cases), although disparities in rates between blacks and non-Hispanic whites have decreased since the 1990s.

Sexual transmission of syphilis occurs primarily through microabrasions in the skin or mucous membranes, which allow entry of treponemes from moist lesions on the penis, mouth, groin, anus, or other locations; most transmission occurs in the primary and secondary stages of the disease.2 Untreated P&S syphilis can result in serious sequelae3; the manifestations of tertiary syphilis include gummatous lesions and cardiac, ophthalmic, auditory, and central nervous system manifestations.4 Congenital syphilis can result in serious and even fatal complications in infants. Syphilis also increases the risk of acquiring and transmitting HIV, further underscoring the importance of prevention.5

Male latex condoms have been recommended as a primary means of preventing sexually transmitted infections (STI) among sexually active individuals.6 A 2001 report by the National Institutes of Health increased awareness of the need to assess the role of condoms in preventing a variety of STIs through well-designed epidemiologic studies.7 While prior systematic reviews have demonstrated that condom use may reduce the risk of several sexually transmitted diseases (STDs), including HIV, gonorrhea, chlamydia, and herpes simplex virus,8–11 there has been no such comprehensive review of condom use and risk of syphilis.

We reviewed publications on syphilis and condoms to describe the available epidemiologic data, systematically evaluate study methods, and provide suggestions for optimal study designs to measure the effect of condom use on risk of syphilis.

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MATERIALS AND METHODS

We searched MEDLINE to identify English-language studies published between January 1, 1972 and May 16, 2008 that assessed the association between male condom use and risk of syphilis. A search was conducted using the keywords “syphilis” or “Treponema pallidum” and “condom” or “condoms,” and the medical subject heading terms “sexually transmitted diseases, bacterial” and “contraceptive devices.” Each abstract from our search was reviewed by at least 2 of the 3 authors (E.D., C.K., and L.W.) to determine which studies to evaluate in full text. Inclusion criteria for studies followed the convention used in an earlier review9; studies had to assess condom use during penile-vaginal or penile-anal intercourse, have a clearly defined control or comparison group, and provide quantitative data on the effect of condom use (or provide data from which an association could be calculated). Studies also had to specify the method of syphilis detection, either by serologic testing or clinical diagnosis. In addition, only studies with at least 7 syphilis cases were included to obtain the most reliable measure of effect. Studies in which the condom use comparison group was not specified and ecological studies were excluded.

For each study included in this review, all 3 authors evaluated design, population size and location, measures of condom use, method of diagnosing syphilis, and measures of association between condom use and syphilis infection. For all measures of association, the lowest level of condom use (e.g., “never use”) served as the referent group and was compared to the highest level of condom use (e.g., “always use”). For studies in which the highest degree of condom use was the reference, we inverted the measure of association provided by the authors. If data were provided with which a measure of association could be calculated, we calculated OR and 95% CI, using OpenEpi.12

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RESULTS

Our search strategy yielded 817 references. All abstracts were reviewed and 245 (30%) studies were selected for evaluation of the full text. Twelve studies met inclusion criteria; 13–24 among the most common reasons for exclusion were the lack of relevant data on syphilis infections according to condom use status, and the inability to distinguish users from nonusers of condoms.

Seven (58%) of the 12 studies were conducted in females only (Table 1), 3 (25%) in males only, and 2 (17%) in both (Table 2). One study provided separate measures of effect for female and male subjects. Nine (75%) studies were cross-sectional, 2 (17%) were prospective cohort studies, and 1 was a case–control study. Seven (58%) studies were conducted among female or male sex workers, while one each was conducted in MSM, male transvestites, STD clinic clients, postpartum patients, and a community population.

Table 1
Table 1
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Table 2
Table 2
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Many different laboratory methods of syphilis detection were used across studies. Only 2 studies evaluated early disease by documenting incident infections.16,19 Laboratory methods included nontreponemal tests (rapid plasma reagin, venereal disease research laboratory, toluidine red unheated serum test) with (n = 5) or without (n = 2) confirmation by a treponemal test (e.g., T. pallidum hemagglutination assay, fluorescent treponemal absorption test). Other studies used a treponemal test alone (n = 2) or ELISA confirmed by T. pallidum particle agglutination test (n = 1). One study classified a positive treponemal or nontreponemal test as evidence of syphilis and 1 study used the 1990 CDC Case Definition for confirmed P&S syphilis or presumptive early latent syphilis.25

Condom use measures also varied widely across studies, and included “always” versus “never,” “always/almost always” versus “never/rarely/sometimes,” “any” versus “no use,” and “consistent” versus “never,” among other comparisons. Eleven (92%) studies evaluated consistent use of condoms (“always” use), either alone or in combination with other measures of use, as in the case of “always/almost always.” The comparison group included, but was not necessarily limited to, “never” use in 8 (75%) studies; other comparison groups included “inconsistent,” “not always,” and “no use” or “nonuse.” No studies assessed correct condom use or condom use problems. The time period over which condom use was assessed did not necessarily correspond with the duration of the study or interval between STD testing and ranged from the past week to the past year, with 3 studies not specifying a time period. Only 2 studies assessed incident syphilis infections.16,19 The remaining 10 studies had insufficient information to distinguish prevalent from incident infections.13–15,17,18,20–24 No studies documented whether subjects had been exposed to infected partners during the period of condom use assessment.

Eleven (92%) studies reported or had sufficient data to calculate a decreased risk of syphilis with condom use, with measures of effect ranging from 0.0 to 0.89 (11%–100% risk reduction); 5 of these studies found a statistically significant reduction in risk15,16,18,23,24 (Tables 1 and 2). Seven (58%) studies presented measures of effect that were adjusted for potential risk factors.13–17,21,23 One study reported an increased risk of syphilis with condom use that was not statistically significant (Adjusted Odds Ratio (aOR) 1.89 [95% CI, 0.98–3.70]) (Table 1).

Two of the most rigorously designed studies were longitudinal assessments of condom use and risk of incident syphilis.16,19 In one study, “always” or “almost always” use of condoms over the past month was associated with a statistically significant reduction in risk of incident syphilis (aOR, 0.39 [95% CI, 0.23–0.64]) compared to use occurring “never,” “rarely,” or “sometimes.”16 In another study, “consistent” users over the past 6 months were compared to “never” users over the past 6 months, according to HIV status.19 In HIV-infected subjects, a nonsignificant reduction in risk of incident syphilis for condom use was found (OR, 0.59 [95% CI, 0.03–4.02]). In HIV-uninfected subjects, there were no incident syphilis infections among consistent condom users, while 9 infections were found among subjects who never used condoms (OR, 0.0 [95% CI, 0–6.44]).

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DISCUSSION

Our review identified 12 studies that assessed condom use and risk of syphilis; most studies, however, did not use sufficiently rigorous methods to accurately assess the association between condom use and reduced risk of syphilis infection. The 2 most rigorously designed studies evaluated in this review both suggested a reduced risk of syphilis; 1 study was statistically significant.

Our review found similar methodologic limitations in studies as other reviews of condom effectiveness.9 Studies used a variety of measures of condom use and some studies18,24 did not clearly distinguish subjects who consistently used condoms from those who inconsistently used condoms, possibly diluting the effect of consistent condom use. In addition, the correct use of condoms and occurrence of use problems were not documented in any studies and the time frame over which condom use was assessed varied widely or was not specified. The duration of the study (and therefore the number of sex acts over time) could also influence the observed measure of effect of condom use; studies of longer duration might be expected to reduce the measure of effect as more sex acts occur and the opportunity for inconsistent and incorrect condom use increases over time.9,26,27 In addition, most of the studies reported a serologic measurement of syphilis which could have indicated either a past or current infection. Finally, studies did not document subjects’ exposure to a partner with an active infection over the time period when condom use was assessed. These last 2 points would tend to bias observed measures of effect toward the null, thereby diminishing any protective effect of condoms.

Measuring the effectiveness of condom use against acquisition of syphilis presents several additional challenges. The infectiousness of syphilis varies with stage, with sexual transmission generally occurring with exposure to primary or secondary lesions.2 In our review, most studies had insufficient information to determine the clinical stage of disease. In addition, syphilis transmission differs from that of many other STIs (e.g., gonorrhea, chlamydia, HIV, and trichomoniasis) in that syphilis also may be transmitted via contact with skin or mucosal surfaces, such as the groin, that are not covered or protected by the condom. Finally, syphilis is rare, making it difficult to study the effect of condoms except in large populations or within specific high-risk populations.

Many serologic tests of varying sensitivity and specificity exist for identification of syphilis. These tests may not distinguish between P&S and latent infections and cannot independently determine which patients are infectious. Many studies included in this review likely identified a clinical state of late latent infection that would have been acquired years earlier. Thus, the selected time period for measuring condom use in the study may not have coincided with the time during which subjects were at risk for and acquired syphilis.

Given the significant methodologic limitations of most reviewed studies on condoms and syphilis, we were unable to calculate a summary estimate of the measure of effect across all studies. Additional studies incorporating rigorous methodologies are needed to further assess the degree to which consistent condom use may reduce the risk of syphilis. Ideally, a study to assess this association would enroll subjects at high risk of syphilis exposure (i.e., sexual contact with a partner with P&S syphilis) in a longitudinal assessment of incident syphilis, with consistent and correct condom use measured with every partner. Such a study could greatly inform prevention efforts, especially in groups who are at high risk of acquiring syphilis, such as MSM in some urban areas.

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REFERENCES

1. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 2006. Atlanta, GA: US Department of Health and Human Services, 2007.

2. Holmes KK, Sparling FP, Stamm WE, et al. Sexually Transmitted Disease. 4th ed. New York, NY: McGraw-Hill Professional, 2007.

3. Danbolt N, Clark E, Gjestland T. The Oslo study of untreated syphilis; a re-study of the Boeck-Bruusgaard material concerning the fate of syphilitics who receive no specific treatment: A preliminary report. Acta Derm Venereol 1954; 34:34–38.

4. Golden MR, Marra CM, Holmes KK. Update on syphilis: Resurgence of an old problem. JAMA 2003; 290:1510–1514.

5. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75:3–17.

6. Centers for Disease Control and Prevention. Sexually Transmitted Disease Treatment Guidelines. MMWR 2006; 55.

7. National Institute of Allergy and Infectious Diseases. Workshop Summary: Scientific Evidence on Condom Effectiveness for Sexually Transmitted Disease (STD) Prevention. Available at: www.niaid.nih.gov/dmid/stds/condomreport. Accessed September, 2001.

8. Holmes KK, Levine R, Weaver M. Effectiveness of condoms in preventing sexually transmitted infections. Bull World Health Organ 2004; 82:454–461.

9. Warner L, Stone KM, Macaluso M, et al. Condom use and risk of gonorrhea and Chlamydia: A systematic review of design and measurement factors assessed in epidemiologic studies. Sex Transm Dis 2006; 33:36–51.

10. Weller S, Davis K. Condom effectiveness in reducing heterosexual HIV transmission. Cochrane Database Syst Rev 2001:CD003255.

11. Casper C, Wald A. Condom use and the prevention of genital herpes acquisition. Herpes 2002; 9:10–14.

12. Open Source Epidemiologic Statistics for Public Health [computer program]. Version 2.2.1. Atlanta, GA: Emory University. Accessed June, 2008.

13. Mejia A, Bautista CT, Leal L, et al. Syphilis infection among female sex workers in Colombia. J Immigr Minor Health. 2009; 11:92–98.

14. Xueref S, Holianjavony J, Daniel R, et al. The absence of HIV seropositivity contrasts with a high prevalence of markers of sexually transmitted infections among registered female sex workers in Toliary, Madagascar. Trop Med Int Health 2003; 8:60–66.

15. van den Hoek A, Yuliang F, Dukers NH, et al. High prevalence of syphilis and other sexually transmitted diseases among sex workers in China: Potential for fast spread of HIV. AIDS 2001; 15:753–759.

16. Levine WC, Revollo R, Kaune V, et al. Decline in sexually transmitted disease prevalence in female Bolivian sex workers: Impact of an HIV prevention project. AIDS 1998; 12:1899–1906.

17. Sanchez J, Gotuzzo E, Escamilla J, et al. Sexually transmitted infections in female sex workers: Reduced by condom use but not by a limited periodic examination program. Sex Transm Dis 1998; 25:82–89.

18. Joesoef MR, Linnan M, Barakbah Y, et al. Patterns of sexually transmitted diseases in female sex workers in Surabaya, Indonesia. Int J STD AIDS 1997; 8:576–580.

19. Taha TE, Canner JK, Chiphangwi JD, et al. Reported condom use is not associated with incidence of sexually transmitted diseases in Malawi. AIDS 1996; 10:207–212.

20. Ruan Y, Li D, Li X, et al. Relationship between syphilis and HIV infections among men who have sex with men in Beijing, China. Sex Transm Dis 2007; 34:592–597.

21. Joesoef MR, Gultom M, Irana ID, et al. High rates of sexually transmitted diseases among male transvestites in Jakarta, Indonesia. Int J STD AIDS 2003; 14:609–613.

22. Gattari P, Speziale D, Grillo R, et al. Syphilis serology among transvestite prostitutes attending an HIV unit in Rome, Italy. Eur J Epidemiol 1994; 10:683–686.

23. Ahmed S, Lutalo T, Wawer M, et al. HIV incidence and sexually transmitted disease prevalence associated with condom use: A population study in Rakai, Uganda. AIDS 2001; 15:2171–2179.

24. Finelli L, Budd J, Spitalny KC. Early syphilis. Relationship to sex, drugs, and changes in high-risk behavior from 1987–1990. Sex Transm Dis 1993; 20:89–95.

25. Centers for Disease Control and Prevention. Case definitions for public health surveillance. MMWR Recomm Rep 1990; 39:1–43.

26. Mann JR, Stine CC, Vessey J. The role of disease-specific infectivity and number of disease exposures on long-term effectiveness of the latex condom. Sex Transm Dis 2002; 29:344–349.

27. Cates W Jr. Contraception, contraceptive technology, and STDs. In: Holmes KK, Sparling PF, Mardh PA, eds. Sexually Transmitted Disease. 3rd ed. New York, NY: McGraw-Hill; 1998:1067–1078.

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