Contact tracing of syphilis-seropositive pregnant women and syphilis-infection among their male partners in Bao'an District, Shenzhen, China

doi:10.21203/rs.3.rs-15971/v1

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Contact tracing of syphilis-seropositive pregnant women and syphilis-infection among their male partners in Bao'an District, Shenzhen, China

https://doi.org/10.21203/rs.3.rs-15971/v1

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Background Untreated male partners are critical source of maternal re-infection. Contact tracing is a good way to identify infection among partners and reduce risk of mother-to-child transmission related to maternal re-infection. This study aimed to analyze the current situation and related factors of contact tracing of syphilis-seropositive pregnant women and syphilis-infection among their male partners.

Method Data of syphilis-seropositive pregnant women and their male partners attending clinics for syphilis-screening were obtained from the Shenzhen Program for Prevention of Congenital Syphilis. Contact tracing rate of syphilis-seropositive pregnant women and syphilis prevalence among male partners were counted, and related factors were also analyzed using a random-effects logistic regression model.

Result Of the 1299 syphilis-seropositive pregnant women, 74.1% (963/1299) had their male partners receiving syphilis-screening and 19.1% (184/963) of male partners were syphilis-infected. For pregnant women, being divorced (adjusted odds ratio [AOR] =0.39; 95%CI: 0.17-0.88), seeking for emergency services at their first antenatal clinics visit (AOR=0.59; 95%CI: 0.44-0.79), reporting willingness to notify partner (AOR=7.75; 95%CI: 4.73-12.70), and having a history of drug abuse (AOR=0.35; 95%CI: 0.13-0.93) were independently associated with successful contact tracing. For male partners, of minority nationality (AOR=4.15; 95%CI: 1.66-10.34), age of first sex>20(AOR=0.57; 95%CI: 0.37-0.87), reporting multi-partner (AOR = 1.60; 95%CI: 1.04-2.46), having a history of drug abuse (AOR=4.07; 95%CI: 1.31-12.64) were independently associated with syphilis-infection. In addition, pregnant women with TRUST titer ≥1:8 (AOR=2.81; 95%CI: 1.87-4.21), having a history of adverse pregnancy outcomes (AOR=1.70; 95%CI: 1.14-2.53), reporting multi-partners (AOR=0.43; 95%CI: 0.29-0.64) and reporting the current partner as the source of syphilis (AOR=5.05; 95%CI: 2.82-9.03) were independently associated with partners' syphilis-infection.

Conclusion Contact tracing is feasible and effective in identifying syphilis-infected partners among syphilis-seropositive pregnant women. Contact tracing is associated with many factors such as women's marital status, services at their first antenatal clinics visit and willingness of partner notification. Partners' ethnicity, age of first sex, multi-partners and history of drug abuse as well as women's levels of TRUST titer were associated with partners' syphilis-infection.

Infectious Diseases

syphilis

pregnancy

contact tracing

partner notification

Despite advances in syphilis prevention of mother-to-child transmission (PMTCT) [1–2], pregnant women face a high risk of syphilis re-infection from infected male partners and adverse pregnancy outcomes (APOs) related to mother-to-child transmission [3–5]. It was estimated that globally there were 355,000 APOs caused by mother-to-child transmission of syphilis in 2016, of which 6% were due to treatment failures or re-infection during pregnancy [2]. Many male partners of syphilis-seropositive pregnant women are also syphilis-infected and do not know their syphilis status [3–4]. Untreated male partners are a critical source of maternal re-infection, and pregnant women with syphilis-infected partners are more likely to have APOs [3, 5].

Contact tracing is the process of notifying index patients' partners of possible exposure, and providing counseling, screening, diagnosis and treatment. As one of the most effective public health interventions in Sexually transmitted disease (STD) management, contact tracing was recommended by the Centers for Disease Control and Prevention (CDC) for all individuals presenting with STD [6]. In many countries, contact tracing was also included as an integral part of PMTCT program to identify partner infection, interrupt transmission, prevent re-infection, and reduce fetus mortality caused by syphilis and HIV infection [3, 4, 7].

In order to prevent mother-to-child transmission (MTCT) of syphilis, the Bureau of Health (now the Health Commission) of Shenzhen Municipality launched a program called the Shenzhen Program for Prevention of Congenital Syphilis (SPPCS) in 2001. All pregnant women are offered free syphilis-screening at their first antenatal clinics visit, and syphilis-seropositive pregnant women are encouraged to bring their male partners for further test and treatment [8]. Using data from the SPPCS, the present study described the current situation of contact tracing of syphilis-seropositive pregnant women and syphilis-infection among their male partners. We also explored factors associated with contact tracing of pregnant women and syphilis-infection among their male partners. Our findings may provide guidance for better contact tracing to identify infection among partners and reduce risk of MTCT related to maternal re-infection.

Recruitment of participants

The Shenzhen Program for Prevention of Congenital Syphilis (SPPCS) is a citywide program supported by the Bureau of Health (now the Health Commission) of Shenzhen Municipality. Initiated in 2001, SPPCS covers all the antenatal clinics (ANCs) in Shenzhen city and offers free syphilis screening for all pregnant women at their first antenatal clinics visit. According to the SPPCS guidelines, syphilis-seropositive was defined as positive results in both toluidine red unheated serum test (TRUST, Shanghai Rongsheng BioTech Co, Ltd, Shanghai, China) and treponemal pallidum particle agglutination (TPPA, Fujirebio Inc, Tokyo, Japan [8]. All syphilis-seropositive pregnant women were encouraged to notify their male partners for further examinations. Three partner notifying approaches were recommended: patient referral, in which the pregnant women notify partners by themselves; provider referral, where doctors notify partners with pregnant women's permission; contract referral, in which pregnant women agree to notify partners, but doctors may intervene if the partners do not present for treatment. Male partners presented to the clinics were recommended for syphilis-screening with both TRUST and TPPA, and if positive, were referred for further treatment [9]. Information of syphilis-seropositive pregnant women and male partner attending clinics for syphilis-screening were collected by the doctor using the structured questionnaire after a written informed consent signed by the participants. The current study samples were drawn from SPPCS datasets and included pregnant women who were syphilis-seropositive and their male partners attending clinics for syphilis-screening in Bao'an District from 2012 to 2017. Considering the relatively stable sex relationships for pregnant women, their male partners traced in this study were limited to the closest one for each pregnant woman, mainly referring to spouse of the married and the closest male partner during the past 12 months for the unmarried or divorced. Syphilis-seropositive pregnant women and their male partners with complete information were finally included for analyses.

SPPCS was approved by the research ethics review committee of the Shenzhen Center for Chronic Disease Control and Prevention. Pregnant women and their male partners were informed of the purpose and details of SPPCS by the doctor and signed an informed consent before participating SPPCS. For data use of the SPPCS for the current study, we obtained an additional ethical review and approval from the committee (approval number 2016NL021). Participants' names, initials, phone numbers and hospital admission numbers did not appear in the text or in illustrative material.

Information collection

According to the SPPCS guidelines [8], standardized medical records of syphilis-seropositive pregnant women were established by the doctor after interviewing with the patients, including: demographic characteristics, behavioral characteristics, obstetric characteristics, clinical characteristics, etc. Information of their male partners presenting to clinics for further examination was also collected by the doctor. Data of pregnant women and their male partners analyzed in the current study included: demographic characteristics (i.e., age, race, education, marital status, occupation, and residency status), behavioral characteristics (i.e., history of drug abuse, history of syphilis or other STDs, age at first sex, number of lifetime sexual partners and condom use),obstetric characteristics (only for pregnant women) (i.e., antenatal care, history of APOs, existing number of children), and clinical characteristics (i.e., syphilitic chancre, polymorphic rash, condylomalata, inguinal lymph nodes).

Statistical Analysis

The primary outcomes of interest included contact tracing rate estimated as the proportion of syphilis-seropositive pregnant women whose partners received syphilis-screening, syphilis prevalence among male partners estimated as the proportion of male partners infected with syphilis, and their 95% confidence interval (CI). We explored potential variables related to contact tracing and syphilis-infection among male partners by using random-effects logistic regression models to estimate unadjusted odds ratio (OR), adjusted odds ratio (AOR) and their 95% CIs. For all analyses, P values < 0.05 were regarded as statistically significant. All analyses were performed using SPSS for Windows software (version 17.0).

Recruitment of participants

Between January 1^st, 2012 and December 31^st,2017, 626 446 pregnant women were screened for syphilis and 1302 were identified to be syphilis-seropositive. A total of 1299 syphilis-seropositive pregnant women with complete available information were enrolled. 963 male partners of syphilis-seropositive pregnant women presented to clinic and received screening for syphilis. Data of 1299 syphilis-seropositive pregnant women and 963 male partners were included for analyses.

Participant characteristics

Characteristics of study participants are presented in Table 1.The pregnant women had a mean age of 28.81 (SD=5.85, range: 16–49), and their partners had a mean age of 31.50 (SD= 6.53, range: 17–56). The pregnant women had a mean gestational week (GW) of 18.08 weeks (SD=10.81, range: 3-41) at their first antenatal, with 605(46.6%) under 13 weeks. Most pregnant women presented to the clinics for routine antenatal care at their first ANCs visit (n=936, 72.1%), and the rest presented for emergency services, including being parturient (n=165, 12.7%), spontaneous abortion (n = 43, 3.3%), stillbirth (n = 25, 1.9%), ectopic pregnancies (n =120, 9.2%), and artificial abortions or inductions (n = 10, 0.8%). Among the 1299 syphilis-seropositive pregnant women, the number of early syphilis, latent syphilis and syphilis after adequate treatment were 10 (0.8%), 870 (67.0%) and 419 (32.3%), respectively. TRUST titer ranged from 1:1-1:256, with the majority under 1:8(n=954, 73.4%).

Contact tracing result

Among the 1299 syphilis-seropositive pregnant women, 1205(92.8%) stated willingness to notify their male partners, and 94 (7.2%) reported that they did not want to notify their male partners. The barriers to partner notify reported by the pregnant women included fear of relationship breakdown (n=82, 87.2%), lack of contact information because of having divorced or separated with partners (n=10, 10.6%), fear of social discrimination (n=1, 1.1%), and distrust of the diagnosis (n=1, 1.1%). 1191 (91.7%) of the syphilis-seropositive pregnant women selected patient referral, 66 (5.1%) selected provider referral and 42 (3.2%) selected contract referral. Finally, 1155(88.9%) pregnant women reported that their partners were notified, 985 (75.8%) partners presented to the clinics and 963 (74.1%) male partners received screening for syphilis, resulting in a contract tracing rate of 74.1% (95% CI, 72.9%-75.3%).

Factor associated with contact tracing

In univariate analyses (Table2), pregnant women being 21-30 years old (OR = 1.99; 95%CI: 1.26-3.15), being unmarried (OR=0.55; 95%CI: 0.40-0.76) or divorced (OR=0.27; 95%CI: 0.13-0.54), length living in Shenzhen being unknown (OR=0.34; 95%CI: 0.18-0.62), unemployment (OR=0.75; 95%CI: 0.58-0.98), GW of the first ANCs visit after 28 weeks (OR=0.62; 95%CI: 0.46-0.85), seeking for emergency services at their first ANCs visit (OR=0.46;95%CI: 0.36-0.60), reporting willingness to notify partner (OR=7.32; 95%CI: 4.65-11.53) and history of drug abuse (OR=0.34; 95%CI: 0.14-0.83) were significantly associated with contact tracing.

In multivariate analyses (Table 2) [see Additional file 1], pregnant women being divorced (adjusted odds ratio [aOR] =0.39; 95%CI: 0.17-0.88), length living in Shenzhen being unknown (AOR =0.38; 95%CI: 0.20-0.73), seeking for emergency services at their first ANCs visit (AOR =0.59; 95%CI: 0.44-0.79), reporting willingness to notify partner (AOR=7.75; 95%CI: 4.73-12.70) and having a history of drug abuse (AOR = 0.35; 95%CI: 0.13-0.93) were independently and significantly associated with contact tracing.

Syphilis infection status among male partners

Among the 963 male partners screened for syphilis, 779 (80.9%) were negative in both TRUST and TPPA, 155 (16.1%) were positive in both TRUST and TPPA, 29 (3.0%) were positive only in TPPA, leading to a syphilis prevalence of 19.1% (184/963). Among the 184 syphilis-infected male partners, the number of early syphilis, latent syphilis and syphilis after adequate treatment were 5 (0.5%), 106 (11.0%) and 73 (7.6%), respectively. TRUST titer ranged from 1:1-1:128, with the majority under 1:8 (n=98, 63.2%).

Factor associated with syphilis infection among male partners

In univariate analyses (Table 3) [see Additional file 1], for pregnant women, TRUST titer ≥1:8 (OR = 1.97; 95%CI: 1.40-2.77), syphilis infection from the current partner (OR = 5.32; 95%CI: 3.16-8.95) or source of infection being unknown (OR = 1.78; 95%CI: 1.05-3.01), multi-partners (OR = 0.39; 95%CI: 0.28-0.56), and history of APOs (OR = 1.62; 95%CI: 1.14-2.30) were all significantly associated with partners' syphilis-infection. For the male partners themselves, minority nationality (OR = 3.14; 95%CI: 1.37-7.19), first sex more than 20 years old (OR = 0.63; 95%CI: 0.44-0.92), and history of drug abuse (OR =2.76; 95%CI: 1.06-7.22) were all significantly associated with their own syphilis-infection.

In multivariate analyses (Table 3), for pregnant women, TRUST titer ≥1:8 (AOR = 2.81; 95%CI: 1.87-4.21), syphilis infection from the current partner (AOR = 5.05; 95%CI: 2.82-9.03), multi-partners (AOR = 0.43; 95%CI: 0.29-0.64), history of APOs (AOR = 1.70; 95%CI: 1.14-2.53) were all independently and significantly associated with syphilis-nfection of their male partners. For the male partners themselves, of minority nationality (AOR = 4.15; 95%CI: 1.66-10.34), age at first sex > 20 years old (AOR = 0.57; 95%CI: 0.37-0.87), multi-partners (AOR= 1.60; 95%CI: 1.04-2.46), and history of drug abuse (AOR =4.07; 95%CI: 1.31-12.64) were all independently and significantly associated with their own syphilis-infection.

Contact tracing was recommended by World Health Organization as a critical strategy of PMTCT [10]. In our study, 74.1% of male partners of syphilis-seropositive pregnant women received further screening for syphilis, similar to the contact tracing rate reported in Bolivia (76.9%) [11], and higher than that reported in Uganda (18%) [12], Peruvian (33.7%) [13], Botswana (52.9%) [4], Kenya (67%) [3] and that reported among non-pregnant women with STD (13.6%-58%) [14–16]. 19.1% of the male partners screened for syphilis were syphilis-seropositive, of whom 60% were newly diagnosed, similar to the prevalence of 18.1% reported in Kenya [3]. The findings indicated the feasibility and efficacy of contact tracing for syphilis among pregnant women.

Consistent with previous studies, partners of pregnant women seeking for routine antenatal care were more likely to present to the clinics for further screening than partners of pregnant women seeking for emergency services due to parturiency, spontaneous abortion, stillbirth, ectopic pregnancy and artificial abortions or inductions. This finding indicates that couples are more compliant with recommendations of partner notification in consideration of their unborn child’s health [3, 13]. Pregnant women's willingness to notify partners was associated with increased contact tracing. Moreover, it was reported in previous studies that poor understanding of disease was one of the barriers to contact tracing [12, 14], and contact tracing among pregnant syphilis patients increased from 29.9–88.8% after counseling [14].These findings suggested that health workers should make it clear to the patients about the potential consequences of syphilis infection for their unborn child and emphasize the importance of partner screening and treatment in preventing APOs caused by re-infection. Compared to married women, divorced pregnant women were more likely to have a casual partner and often did not inform their partners or could not trace casual partners [3, 17].

Compared to those having first sex before 20 years old, partners having first sex after 20 usually had higher self-protection awareness, which decreased risk of syphilis-infection. Compared to Han, other ethnicities (mainly Zhuang, Miao and Yao) were mostly rural-to-urban migration workers with increased risk of acquiring STIs due to insufficient reproductive health knowledge and inadequate health services utilization [18–19]. Multi- partners and drug abuse were risk factors of acquiring STD. Drug abusers were involved in risk behaviors that may place them at increased risk of STD, such as promiscuity, multi-partners and unprotected sex. Moreover, intravenous drug use also increased risk of STD by blood-borne infection.

Historical data suggest that patients with high TRUST titers, as seen in earlier stages of infection, were most at risk of passing on infection to their partners, and the risk of transmission decreased with the duration of infection [20–21]. Women with TRUST titer ≥ 1:8were highly infectious and more likely to transmit to their partners. On the other hand, as the infected women with TRUST titer ≥ 1:8 were more likely to be in earlier stages of infection, indicating new infection from the current relationship. Compared to pregnant women with multiple sex partners, women with only one sex partner were more likely to be infected from the current partners. For pregnant women with a history of APOs, partner screening should be valued and strengthened although the association between APOs and partners' syphilis-infection have not been checked.

Our study had several limitations. First, successful contact tracing depends on both partner notify and partner compliance. In the current study, we recruited male partners through pregnant women and analyzed only those presented to the clinics. Information of those who didn’t present to the clinics remains unknown. Second, male partner traced in our study were limited to spouse of married pregnant women and the closest male partner of the unmarried or divorced pregnant women. Future research may consider expanding partners by including casual sex partners with exposure risks to identify more cases and further reduce re-infection. However, the study provides implications for further interventions to improve pregnant women’s contact tracing and identify syphilis-infection in partners to reduce risk of mother-to-child transmission related to maternal re-infection.

In this study, we found that 74.1% of male partner received further syphilis-screening and 19.1% of them were syphilis-seropositive, confirming feasibility and effectiveness of contact tracing for syphilis among pregnant women. Contact tracing was affected by many factors, including pregnant women's marital status, services at their first ANCs visit and willingness of partner notify. Partners' syphilis infection was associated with pregnant women's TRUST titer, partners' ethnicity, drug abuse, age of first sex, as well as multi-partners. These findings provide implications for better contact tracing to identify infection among partners and reduce risk of mother-to-child transmission related to maternal re-infection.

PMTCT: Prevention of Mother-To-Child Transmission; APOs: Adverse Pregnancy Outcomes; STD: Sexually transmitted disease; CDC: Centers for Disease Control and Prevention; MTCT: Mother-To-Child Transmission; SPPCS: Shenzhen Program for Prevention of Congenital Syphilis; ANCs: Antenatal Clinics; TRUST: Toluidine Red Unheated Serum Test; TPPA: Treponemal Pallidum Particle Agglutination; CI: Confidence Interval; OR: Odds ratio; AOR: Adjusted Odds Ratio; GW: Gestational Week.

Ethics approval and consent to participate

SPPCS was approved by the research ethics review committee of the Shenzhen Center for Chronic Disease Control and Prevention. For data use of the SPPCS for the current study, we obtained an additional ethical review and approval from the committee (approval number 2016NL021).

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This study was supported by Fundamental Research Project of Medical Health in Bao'an District (project number 2018JD174). The funders had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Authors' contributions

Rui-Lin Yan and Zhi-Ming Huang conceived and designed the study. Rui-Lin Yan, Bao-Qing Deng, Gui-Chun Wen, Li-Cheng Huang and Li-Mei Li collected the data. Rui-Lin Yan analyzed and interpreted the data, and drafted the article. Rui-Lin Yan and Zhi-Ming Huang revised the article.

Acknowledgments We thank all the doctors, nurses, laboratory and data teams and the administrative and support staff in antenatal clinics participated SPPCS.

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Table 1 Characteristics of syphilis-seropositive pregnant women and male partners

Characteristics	Pregnant women n (%)	Male partners n (%)
Age (Years)
≤ 20	94(7.2)	22 (2.3)
21-30	308(53.5)	443 (46.0)
31-40	387(37.2)	403 (41.8)
>40	334(2.1)	95 (9.9)
Ethnicity
Han	1252(96.4)	939 (97.5)
Others	47(3.6)	24 (2.5)
Marital status
Unmarried	203(15.6)	-
Divorced	32(2.5)	-
Married	1064(81.9)	-
Household register
Shenzhen	45(3.5)	78 (8.1)
Non-Shenzhen	1254(96.5)	885 (91.9)
Length living in Shenzhen (Years)
≤2	366(28.2)	172 (17.9)
＞2	885(68.1)	768 (79.8)
Unknown	48(3.7)	23 (2.4)
Occupation
Worker	267(20.6)	516 (53.6)
Server	36(2.8)	39 (4.0)
Office clerk	88(6.8)	149 (15.5)
Individual operator	72(5.5)	219 (22.7)
Unemployment	836(64.4)	40 (4.2)
Education level
Secondary school or below	895(68.9)	489 (50.8)
Senior high school	301(23.2)	326 (33.9)
College or above	103(7.9)	148 (15.4)
History of APOs
Yes	302(23.2)	-
No	997(76.8)	-
History of drug abuse
Yes	20(1.5)	18 (1.9)
No	1279(98.5)	945 (98.1)
History of other STD
Yes	14(1.1)	8 (0.8)
No	1285(98.9)	955 (99.2)
Age of first sex (Years)
≤20	418(32.2)	429 (44.5)
＞20	881(67.8)	342 (35.5)
Unknown	0 (0.0)	192 (19.9)
Number of lifetime sex partners
1	478 (36.8)	311 (32.3)
≥2	652 (50.2)	377 (39.1)
Unknown	169 (13.0)	275 (28.6)
Condom use with current partner
Never use	384(29.6)	-
Sometimes use	781(60.1)	-
Frequently use	134(10.3)	-
Source of syphilis infection on pregnant women's reports
Current partners	379(29.2)	-
Someone other than current partner	296(22.8)	-
Unknown	624 (48.0)	-

Table 2 Logistic model of factors associated with contact tracing among syphilis-seropositive pregnant women

(See Additional file 1)

Table 3 Logistic model of factors associated with syphilis-infection among male partners (See Additional file 1)

Additional files

Additional file 1

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Contact tracing of syphilis-seropositive pregnant women and syphilis-infection among their male partners in Bao'an District, Shenzhen, China

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