Prevalence of syphilis infection and associated sociodemographic factors among antenatal-care attendees in Meghalaya,India: Revisiting HIV Sentinel Surveillance data

Abstract

Background

Despite relatively simple prevention and treatment, syphilis remains a major social and public health concern worldwide, particularly in developing nations.

Objective

To estimate the prevalence and to determine the sociodemographic factors associated with syphilis infection among antenatal-care (ANC) attendees in Meghalaya, India.

Materials and Method

A facility-based cross-sectional study was conducted utilizing National HIV Sentinel Surveillance of Meghalaya, January–March 2017. Pregnant women aged 15–49 years (n = 3015) were recruited consecutively, interviewed, and tested for syphilis by Venereal Disease Research Laboratory test in eight selected ANC sites representing all districts of Meghalaya.

Results

Prevalence of syphilis was found to be 1.03 % (95% CI = 0.67–1.39) (31/3015). Prevalence was maximum among illiterates with gradual lowering of adjusted odds ratio (AOR) with improvement of education. Women whose husbands had no income were associated with higher risk (AOR = 4.97, 95% CI = 1.11–22.20) of syphilis. Significant risk (OR = 2.42, 95% CI = 1.02–5.74) was also observed with Jaintia Hills residents as compared to Garo Hills.

Conclusions

As high prevalence of gestational syphilis was identified in Meghalaya along with important sociodemographic predictors, evidence to policy translation is required at state and national level to scale up prevention, screening, and management of syphilis

Keywords

Syphilis sociodemographic factors pregnant women Sentinel Surveillance Meghalaya

Introduction

Sexually transmitted diseases (STDs) are widespread in the third world and constitute a major public health problem in India.¹ Syphilis, caused by the spirochete Treponema pallidum, is one of the most lethal STDs transmitted through sexual intercourse via genital, oral, and anal routes^2,3 as well as through transfusion of contaminated blood and blood products and sharing of needles during drug injection.⁴ The 2008 WHO worldwide estimate showed approximately 1.4 million pregnant women (approximately 1% of total pregnancies) had “probable active syphilis” or syphilis infection sufficiently active to result in mother-to-child transmission (MTCT)⁵ and over a million pregnant women acquire syphilis infection each year globally.⁶ Thus, despite its relatively simple prevention and treatment, syphilis remains a major social and public health concern worldwide.

Inadequately treated or untreated maternal syphilis often result in adverse pregnancy outcomes such as stillbirth, late fetal loss, neonatal death, and premature and low birth weight infants, while congenital syphilis contributes to a substantial burden in respect to health outcome and productivity.⁷ Syphilis-infected mothers are more than twice as likely to have adverse pregnancy outcomes than uninfected mothers and that early intervention in the first and second trimesters of pregnancy significantly reduced MTCT.⁸ There are indications that prevalence of congenital syphilis is declining due to increased efforts to screen and effective treatment of pregnant women for syphilis. The risk of acquisition of syphilis and other Sexually transmitted infections (STIs) are driven by a spectrum of biological and behavioral attributes. Antenatal-care (ANC) services are the target point for prevention of MTCT (PMTCT) initiatives and ideal for monitoring their progress.

One of the eight states of North East India, Meghalaya, is bounded on the north, east, and west by Assam and shares an international border with Bangladesh on the south. There was a steady increase in the total HIV burden in Meghalaya since 2007—to 28% in total HIV/AIDS cases during the last 8 years. The 15th round of HIV Sentinel Surveillance (HSS) among ANC attendees, which was held in 2017, has shown an increase in HIV prevalence. Recent data demonstrated that there had emerged new hotspots of HIV and STDs in Meghalaya along with other North Eastern states of India.^9,10 It was also noted that a pocket of high prevalence with more than 1% had been observed among pregnant women in predominantly Jaintia Hills district followed by East Khasi Hill district. Data from National AIDS Control Organization (NACO) in India showed a declining trend of sero-positivity of syphilis among ANC attendees from 1.7% in 2005–2006 to 0.8% in 2010–2011 and 0.10% in 2016–2017.^9,10 However, estimates at the sub-national level may be more useful for program planning and implementation for PMTCT of syphilis¹¹ as the prevalence of syphilis has been shown to vary across geographic areas, study population, and time period.^12,13 Thus, it is imperative to conduct epidemiological studies at the sub-national level, that is, state level, eventually scaling down to district levels. Monitoring the “at-risk” groups, especially ANC attendees, is essential for guiding clinical action, resource allocation, and intervention programs to make progress toward eliminating this dreaded disease.

Syphilis screening in early stage as well as treatment among ANC attendees, improving partner management, and reducing syphilis prevalence in the general population will be required to achieve global congenital syphilis elimination. Although the prevalence of syphilis in the North Eastern states of India is higher than the national average,¹⁰ there is a dearth of data, specifically regarding the sociodemographic factors associated with the acquisition of syphilis in these areas. The objective of this study was to estimate the prevalence and to determine the sociodemographic factors associated with syphilis infection among antenatal-care attendees in the North Eastern state of Meghalaya, based on analysis of HSS data of this region.

Materials and method

Ethics statement

All procedures of HSS were conducted following the “linked anonymous testing” strategy approved by Ethical Committee of NACO, New Delhi, India. The study involving human participants was in compliance with the Helsinki Declaration. Privacy and confidentiality were maintained throughout the study. All data were recorded anonymously without any personal identifiers. The Institutional Ethics Committee, ICMR-National Institute of Cholera and Enteric Diseases, Kolkata, India, also approved the study.

Study design

A facility-based cross-sectional study was conducted utilizing HSS 2017 data from the state of Meghalaya, India. In the HSS program, targeted project intervention sites (known as sentinel sites) were established in every state for surveillance and monitoring and subsequent strengthening of ongoing prevention services. HSS data were collected from all designated sentinel sites (8 in number) representing all districts of Meghalaya.

Sample size estimation and sampling method

With the assumption of 1.7% prevalence of syphilis among pregnant women,¹⁴ 0.5% acceptable margin of error, and 95% confidence level, the estimated sample size amounts to 2561 (Epi Info V7, CDC). In HSS, the recruitment continued until the target sample size of 400 from each site was reached or stipulated time period of three months were over. Thus, from eight HSS sites of Meghalaya, a total of 3015 eligible pregnant women were recruited and considered for analysis.

Pregnant women aged between 15 and 49 years on their first visit to the designated HSS sites during the surveillance period (January–March 2017) were enrolled for the study in concurrence to the NACO guidelines.¹⁵ Recruitment was done through consecutive sampling of pregnant women independent of the date of antenatal registration, earlier syphilis sero-positivity status (if known), and participation in the surveillance in previous rounds.

Data collection

After recruitment, upon receipt of consent, a face-to-face interview was conducted through predesigned, pre-tested, semi-structured questionnaire by trained health personnel adhering to privacy and confidentiality protocols established by NACO. Information was collected on sociodemographic characteristics such as age, education, residential area, current occupation of the respondent, current occupation of the spouse, and history of spouse residing alone at a different geographical location for more than six months. Additionally, data related to current pregnancy and uptake of ANC services such as order of current pregnancy, source of referral to the ANC clinic, etc. were also elicited. Database management and data quality assurance were stringently maintained as per the NACO protocols.

Syphilis testing

Blood was collected from the enrolled subjects by venipuncture following standard protocols. A linked anonymous testing strategy was adopted to ensure that the participants who tested positive could be traced back and offered treatment. The algorithm used in the National HIV Sentinel Surveillance 2017 in India was the standardized Venereal Disease Research Laboratory (VDRL) test for syphilis screening and estimation of syphilis prevalence among ANC attendees. All the samples were subjected to VDRL testing using standard method at designated HSS testing laboratories. For samples that yielded positive results in the qualitative VDRL test, quantitative VDRL testing was performed using 1:8 dilutions of the sera. All syphilis-positive and 5% of the syphilis-negative sera samples selected randomly were sent to the National Reference Laboratory (NRL) located at the ICMR-National Institute of Cholera and Enteric Diseases, Kolkata. NRL independently rechecked syphilis status of the sera samples as a quality control mechanism under the External Quality Assurance Scheme.

Data analysis

Following data compilation and data cleaning, multiple logic checks were done as a part of data quality assurance. Data analyses were done using SAS version 9.3.2. Descriptive analyses were conducted to determine the prevalence (with 95% confidence interval) and distribution of syphilis sero-positive cases across various sociodemographic characteristics. Univariate (unadjusted) and multivariate (adjusted for potential confounders) logistic regression analyses were performed to determine the associations between various sociodemographic characteristics/order of pregnancy and syphilis risk.

Results

Out of total 3015 pregnant women screened, 31 were found sero-positive for syphilis, thereby prevalence being 1.03% (95% CI = 0.67–1.39). Mean age of the study participants was 25.58 years (SD ± 5.61). The majority of the respondents were in the age group of 15–24 years (48.56%), were educated up to secondary level (44.80%), and resided in rural areas (87.73%). Most of the respondents and had “no income” (82.49%) and 58.81% of the respondents’ husbands had “irregular income.” In relation to the pregnancy profile and healthcare seeking, 28.43% were primigravida, 64.70% visited antenatal clinic by their own decision, and 28.63% were referred by from public healthcare providers (Table 1).

Table 1.

Distribution of the sociodemographic factors, pregnancy-related attributes, and syphilis sero-positivity in overall and different strata among ANC attendees in Meghalaya, India, January–March 2017.

Categorical variables	Total		Syphilis positive
Categorical variables	N	Percentage (95%CI)	N	Prevalence (95% CI)
Overall	3015	—	31	1.03 (0.8–1.4)
Age group
15–24	1464	48.56 (46.8–50.3)	16	1.09 (0.6–1.6)
25–34	1257	41.69 (39.9–43.4)	12	0.95 (0.4–1.5)
≥35	294	9.75 (8.7–10.8)	3	1.02 (0.0–2.2)
District
Garo Hills	1018	33.76 (32.1–35.4)	8	0.79 (0.2–1.3)
Jaintia Hills	797	26.43 (24.9–28.0)	15	1.88 (0.9–2.8)
Khasi Hills	800	26.53 (25.0–28.1)	7	0.88 (0.2–1.5)
Ri Bhoi	400	13.27 (12.1–14.5)	1	0.25 (0.0–0.7)
Education
Illiterate	462	15.35 (14.1–16.6)	13	2.81 (1.3–4.3)
Literate and< = 5	723	24.03 (22.5–25.6)	5	0.69 (0.1–1.3)
Secondary	1348	44.80 (43.0–46.6)	10	0.74 (0.3–1.2)
Higher secondary and above	476	15.82 (14.5–17.1)	3	0.63 (0.0–1.3)
Order of current pregnancy
First	856	28.43 (26.8–30.0)	8	0.93 (0.3–1.6)
Second	760	25.24 (23.7–26.8)	8	1.05 (0.3–1.8)
Third	507	16.84 (15.5–18.2)	6	1.18 (0.2–2.1)
Fourth or more	888	29.49 (27.9–31.1)	9	1.01 (0.4–1.7)
Duration of pregnancy
First trimester	898	29.82 (28.2–31.5)	11	1.22 (0.5–1.9)
Second trimester	1378	45.77 (44.0–47.5)	17	1.23 (0.7–1.8)
Third trimester	735	24.41 (22.9–25.9)	3	0.41 (0.0–0.9)
Source of referral to the ANC clinic
Self-referral	1930	64.70 (63.0–66.4)	19	0.98 (0.5–1.4)
Family/relatives/neighbors/friends	199	6.67 (5.8–7.6)	1	0.50 (0.0–1.5)
Govt (including, ASHA/ANM)	854	28.63 (27.0–30.2)	11	1.29 (0.5–2.0)
Residential area
Urban	366	12.27 (11.1–13.4)	2	0.55 (0.0–1.3)
Rural	2616	87.73 (86.5–88.9)	29	1.11 (0.7–1.5)
Current occupation of the respondent
Regular income	234	7.76 (6.8–8.7)	3	1.28 (0.0–2.7)
Irregular income	294	9.75 (8.7–10.8)	7	2.38 (0.6–4.1)
No income	2487	82.49 (81.1–83.8)	21	0.84 (0.5–1.2)
Current occupation of the spouse
Regular income	1108	37.04 (35.3–38.8)	7	0.63 (0.2–1.1)
Irregular income	1759	58.81 (57.0–60.6)	21	1.19 (0.7–1.7)
No income	124	4.15 (3.4–4.7)	3	2.42 (0.0–5.1)
Spouse resided alone at another place>6 months
Yes	20	0.67 (0.4–1.0)	1	5.00 (0.0–14.6)
No	2967	99.33 (99.0–99.6)	30	1.01 (0.7–1.4)

Among the 31 women who tested sero-positive for syphilis, mean age was 25.06 years (SD ± 5.05). Syphilis sero-prevalence was highest among women aged 15–24 years (1.10%), followed by those >35 years (1.03%) and 25–34 years (0.96%). The ANC attendees from the Jaintia Hills district showed maximum prevalence (1.88% (95% CI = 0.94–2.83)) followed by those from by Khasi Hills district (0.88% (95% CI = 0.23–1.52)) and Garo Hills district (0.79% (95% CI = 0.24–1.33)). Syphilis prevalence was highest (2.81%) among illiterates which is the maximum prevalence in any of the subgroups under study. Prevalence was lowest (0.93%) among primigravidae and increased to >1% among women with higher parity. Subgroups with rural residence (1.12%), irregular income of self (2.38%), and no income of spouse (2.42%) showed higher syphilis prevalence compared to other subgroups (Table 1).

On univariate analysis, statistically significant association was observed for the district of residence, education status, and lack of income of the spouse. Being residents of the Jaintia Hills district was associated with >2 times risk of acquiring syphilis as compared to residence in Garo Hills (OR = 2.42, 95% CI = 1.02–5.74). We found highest prevalence of syphilis infection among illiterates, thus keeping illiterates as reference and significant lowering of odds was observed with the improvement of education status. This association persisted even after adjustment of confounders by multivariate methods (up to fifth standard AOR = 0.27, 95% CI = 0.09–0.84; secondary level AOR = 0.25, 95% CI = 0.09–0.68; high secondary and above AOR = 0.15, 95% CI = 0.03–0.72). Risk of syphilis sero-positivity was almost five times even after adjustment of confounders among women whose husbands had no income (AOR = 4.97, 95% CI = 1.11–22.20) compared those whose husbands had regular income. Rural residents (OR = 2.04, 95% CI = 0.49–8.59) had twice the risk of being syphilis positive, but statistical significance was not seen. For the other sociodemographic variables, statistically significant associations were not noted (Table 2).

Table 2.

Association between sociodemographic, pregnancy-related attributes, and syphilis sero-positivity among ANC attendees in Meghalaya, India, January–March 2017.

Categorical variable	Categories	Unadjusted			Adjusted
Categorical variable	Categories	OR	95% CI	p value	OR	95% CI	p value
Age group	15–24	Reference			Reference
	25–34	0.87	0.4–1.5	0.72	0.77	0.3–2.0	0.58
	≥35	0.93	0.3–3.2	0.91	0.73	0.1–3.5	0.69
District	Garo Hills	Reference			Reference
	Jaintia Hills	2.42	1.0–5.7	0.04	1.72	0.6–4.8	0.30
	Khasi Hills	1.11	0.4–3.1	0.83	1.64	0.5–5.0	0.39
	Ri Bhoi	0.32	0.0–2.5	0.28	0.33	0.0–3.0	0.32
Education	Illiterate	Reference			Reference
	Literate and< = 5	0.24	0.1–0.7	0.01	0.27	0.1–0.8	0.02
	Secondary	0.26	0.1–0.6	0.00	0.25	0.1–0.7	0.00
	Higher secondary and above	0.22	0.1–0.8	0.02	0.15	0.0–0.7	0.02
Order of current pregnancy	First	Reference			Reference
	Second	1.13	0.4–3.0	0.81	1.18	0.4–3.4	0.76
	Third	1.27	0.4–3.7	0.66	1.22	0.4–4.0	0.75
	Fourth or more	1.09	0.4–2.8	0.87	0.74	0.2–2.8	0.66
Duration of pregnancy	First trimester	Reference			Reference
	Second trimester	1.01	0.5–2.2	0.99	1.10	0.5–2.4	0.81
	Third trimester	0.33	0.1–1.2	0.09	0.32	0.1–1.2	0.09
Source of referral to the ANC clinic	Self-referral	Reference			Reference
	Family/relatives/neighbors/friends	0.51	0.1–3.8	0.51	0.61	0.1–5.1	0.64
	Govt (including, ASHA/ANM)	1.31	0.6–2.8	0.47	1.14	0.5–2.6	0.76
Residential area	Urban	Reference			Reference
Residential area	Rural	2.04	0.5–8.6	0.33	1.69	0.4–7.8	0.50
Current occupation of the respondent	Regular income	Reference			Reference
	Irregular income	1.88	0.5–7.3	0.36	0.64	0.1–3.3	0.59
	No income	0.66	0.2–2.2	0.50	0.33	0.1–1.3	0.11
Current occupation of the spouse	Regular income	Reference			Reference
	Irregular income	1.90	0.8–4.5	0.14	1.09	0.4–2.9	0.87
	No income	3.9	1.0–15.3	0.05	4.97	1.1–22.2	0.03
Spouse resided alone at another place>6 months	Yes	Reference			Reference
Spouse resided alone at another place>6 months	No	0.19	0.0–1.5	0.11	0.14	0.0–1.2	0.08

Discussion

The syphilis sero-positivity among 3015 pregnant women assigned to HSS sites in Meghalaya during 2017 was estimated to be 1.03% (0.67–1.39%), which was higher among those women with lower educational levels and those from families with no or unregular income. Meghalaya’s prevalence of syphilis among pregnant women was the highest among all the states in India and much higher than the national level prevalence.¹⁰ Most other North Eastern states also had syphilis prevalence higher than the national average including Tripura (0.88%), Nagaland (0.26%), Manipur (0.13%), and Arunachal Pradesh (0.13%).¹⁰ Keeping the current slowly declining trend of syphilis among ANC attendees in this country in mind, this alarmingly high syphilis, as well as HIV burden among ANC attendees in Meghalaya, might be considered as one of the greatest public health concerns. Previous studies from different regions of India reported a prevalence of around 1% (1.7% in Punjab, 1.4% in Andhra Pradesh, and 0.7% in Kerala) among pregnant as well non-pregnant women attending health facilities.^14,16,17

We observed literacy to be a significant predictor of syphilis infection with gradual lowering of risk with the enhancement of education level. Association of syphilis with low education levels has been reported by earlier studies from India¹⁴ and other countries.^18–21 Higher education may reduce risk by enhanced awareness of the couple about safe sexual practices, higher health-seeking behavior, and adherence to health advisory.

Association of the area of residence (unadjusted) and spouse`s income with syphilis infection was also elicited in this study. Approximately 48% (15 cases) of the syphilis sero-positive individuals in our study resided in the Jaintia Hills district. This is the easternmost part of the state, sparsely populated, and a major site for coal mining in the state. Along with poverty, lack of access to healthcare facilities and poor knowledge about STIs and safe sex practices might be important contributors to higher prevalence in these difficult to access sites.²² As per the District Level Household & Facility Survey - 4 (2012–2013), only 5.1% women from Jaintia Hills district had any knowledge of STIs.²³ As reported for the state of Meghalaya, only 19.8% (urban 23.2% and rural 18.7%) women of reproductive ages (15–49 years) have ever undergone examination of cervix and 47% (urban 57.4 % and rural 43.6 %) women were aware that consistent condom use can reduce the chance of getting HIV/AIDS.²⁴ Meghalaya has also shown an increasing prevalence of HIV infections, with a 10% increase in new infections between 2010 and 2017.²⁵ The impact of low literacy and poverty falls upon overall reproductive morbidity, particularly in rural communities.²⁶ There is an estimated 2- to 5-fold increased risk of acquiring HIV if exposed to that infection when syphilis is present, and studies have also shown that syphilis will increase the viral load of someone who is already infected.¹⁸ Recent data from national HIV surveillance in India showed increasing trend of HIV prevalence in these emerging hotspots.²⁷ HIV-associated risk behavior also increases acquiring of sexually transmitted infection.

Some sociodemographic factors did not show statistically significant associations owing to small number of sero-positive syphilis cases in our study but were still considered critical in the transmission and epidemiology of syphilis and other STDs. Among this, high prevalence in younger age group was in concordance to past literature.^18,19,27 However, one study reported higher prevalence of syphilis among older women.²⁸ Lumbiagnon et al. concluded that for syphilis, younger age was associated with higher incidence while older age was associated with higher prevalence.²⁹ Migration status of the spouse has also been perceived as a major risk factor for acquiring and transmitting STIs (including syphilis), with these individuals as bridge population owing to their geographical mobility and probability of contact with commercial sex workers.³⁰

Limitations of this study include the small number of positive samples obtained. Additionally, being a cross-sectional study, causal associations could not be extrapolated. The HSS data did not have any information on behavioral factors including sexual behavior of the ANC attendees or their partners, so the role of these factors could not be evaluated. VDRL was used as the screening test for syphilis in the HSS program and our prevalence results are based on these findings; confirmatory tests such as Treponema pallidum Haemaggultination were beyond the scope of this program.

Despite these limitations, by virtue of large representative sample size for estimating prevalence, good quality data, sound methodology, and statistical analyses, the findings from this present study yielded useful information regarding distribution and predictors of syphilis sero-positivity among ANC attendees in the North Eastern part of India. Such evidence may be useful to direct policy formulation, group-specific intervention strategy development, and targeted implementation of the prevention programs. Client-oriented, need-based, demand-driven health education strategies; income generation and empowerment approaches and scaling up the STI prevention; and screening and management are highly felt required to address the high burden of syphilis in Meghalaya.

Conclusion

High prevalence of gestational syphilis was identified in Meghalaya along with important its sociodemographic predictors. Evidence to policy translation is highly required at state as well as national level to ensure screening of all pregnant women for syphilis. Early detection should be linked to programs for PMTCT of STIs. Community-based syphilis prevention efforts should be reinforced, especially at the difficult to reach remote locations. Rollout of the syphilis control programs specifically targeting the high-risk ANC attendees is crucial in Meghalaya, specifically in the Jaintia Hills district for preventing the spread of the disease within this vulnerable population.

Footnotes

Acknowledgments

The authors sincerely acknowledge the Project Director, the officials of Meghalaya State AIDS Prevention & Control Society for their whole hearted support in conducting the study.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Contributorship

SB, PG, DC - Conceptualized and designed the study, collected, analyzed and interpreted the data. Written the manuscript and reviewed critically. FD, MKS, SD - Contributed in designing, literature review, data analysis and interpretation. Written and reviewed the manuscript critically.

ORCID iDs

Debjit Chakraborty

Malay Kumar Saha

Shanta Dutta

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