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, 12:69 | Cite as

Seroprevalence of syphilis and its risk factors among pregnant women attending antenatal care at Felege Hiwot Referral Hospital, Bahir Dar, northwest Ethiopia: a cross-sectional study

  • Kiros Tareke
  • Abaineh MunsheaEmail author
  • Endalkachew Nibret
Open Access
Research note

Abstract

Objective

The objective of this study was to investigate the seroprevalence and associated risk factors of syphilis among pregnant women attending antenatal care at Felege Hiwot Referral Hospital, northwest Ethiopia.

Result

Of the total 384 screened women for syphilis, 10 (2.6%) were found to be seropositive for Treponema pallidum. The odds of infection were about ten times (COR = 9.77, p = 0.002) higher in divorced women than in married women. The likelihood of syphilis was almost three times higher among rural residents compared to urban residents (COR = 3.48, p = 0.079). The likelihood of being infected with syphilis was about five times higher (COR = 5.25, p = 0.018) in women who had prior history of multiple sexual partners. The risk of syphilis was 4.42 (p = 0.071) and 2.67 fold (p = 0.226) greater in women with previous history of abortion and other sexually transmitted diseases (STDs), respectively. It can be concluded that a relatively low seroprevalence of syphilis was observed among the study subjects. Nevertheless, health promotion activity directed at raising the awareness of the community towards the modes of transmission of syphilis and its health impact is important in the prevention of the disease in pregnant women.

Keywords

Pregnant women Risk factors Seroprevalence Syphilis 

Abbreviations

AIDS

Acquired Immunodeficiency Syndrome

ANC

antenatal clinic

CI

confidence interval

COR

crude odds ratio

ETB

Ethiopian Birr

FHRH

Felege Hiwot Referral Hospital

HIV

human immunodeficiency virus

ICS

immunochromatography test strips

RPR

rapid plasma reagin

STIs

sexually transmitted infections

WHO

World Health Organization

Introduction

Syphilis is a sexually transmitted infectious disease caused by the bacterium Treponema pallidum and it spreads most commonly through sexual activity. In addition, it can also be transmitted from infected pregnant women to their unborn children. If syphilis is left untreated, it can lead to devastating fetal outcomes in the second or third trimesters of pregnancy [1, 2].

Despite the availability of inexpensive and effective antibiotic therapy, syphilis remains a prevalent disease in developing countries and has re-emerged as a public health threat in developed nations [3]. An estimated 36 million people are infected with syphilis worldwide, with 12 million new infections are reported every year, and of which 2 millions are pregnant women. More than half of infected women transmit the infection to their babies resulting in adverse pregnancy outcomes including early fetal death, stillbirth, preterm birth, low birth weight, neonatal death, and congenital infection in infants [4, 5, 6]. In Africa, seroprevalence of syphilis ranges from 4 to 15% among antenatal clinic attendees and it contributes to approximately 20% of prenatal deaths [7, 8, 9].

Variations in socio-demographic characteristics, sexual practices and behavior of the communities, inaccessibility to treatment of sexually transmitted diseases (STDs) and cultural practices are amongst the risk factors associated with syphilis [10, 11, 12].

Ethiopia is one of resource constrained countries in the world and shows no continuous effort in generating epidemiological data about syphilis and its associated risk factors among pregnant women. In view of this, we undertook this study to determine the seroprevalence of syphilis among pregnant women attending antenatal care at Felege Hiwot Referral Hospital (FHRH), Bahir Dar, Ethiopia.

Main text

Methods

Study design and area

Hospital based prospective cross-sectional study was conducted among pregnant women attending antenatal clinic (ANC) at FHRH. All newly registered pregnant women at ANC of the hospital were considered as a source population, while those who visited the center during sample collection period (November 2013 to June 2014) were considered as a study population.

Bahir Dar is the capital city of Amhara National Regional State and is located at 11°36′ latitude N and 37°23′ longitude E in north-western part of Ethiopia with an altitude of 1800 m. According to Amhara Bureau of Finance and Economic Development 2014 report, population of Bahir Dar city was estimated to be 284,020, of which 134,818 are males and 149,202 are females [13]. Among females, 93,174 of them are between 15 and 49 years of age (reproductive age groups).

Sample size estimation and sampling technique

The minimum sample size, 384 study subjects, was calculated using a single population proportion formula, with 95% confidence interval, 5% margin of error, and 50% prevalence [14]. Then, every eligible pregnant woman was included in the study through simple random sampling technique until the required sample size was obtained.

Data collection and processing

Questionnaire was administered to every eligible consented woman to gather data on socio-demographic characteristics, gestational age, parity status, sexual behavior, and awareness toward syphilis.

After administering the questionnaire, five milliliters of venous blood sample was drawn from each of the study participant and put into plain vacutainer tubes. Sera were then separated from the whole blood by centrifugation at 3000 rpm for 5 min and transferred into labeled tubes and kept at − 20 °C for further laboratory analysis.

Serological analyses of serum samples were carried with two types of diagnostic kits according to the manufacturers’ instructions and recommendations. The sera were initially tested with Rapid Plasma Reagin (RPR) card test to detect non-Treponemal antibodies. Positive and negative controls were included in the assays. All RPR positive sera were subjected to Immunochromatography test strips (ICS) as a confirmatory test. When RPR and ICS tests are positive, then the subject is considered as syphilis positive.

Data analysis and interpretation

Questionnaire and serodiagnosis data were analyzed using SPSS version 20. Chi square (χ2) test was conducted to determine the association between syphilis and risk factors. Then, strength of association in terms of crude odds ratio (COR) between syphilis and risk factors was analyzed using univariate logistic regression.

Results

Socio-demographic variables

The mean age and age range of subjects were 26.95 and 18–44 years old, respectively. Majority (73.7%) of participants were in the age group of 20 to 29 years old. Most of them were married (93.2%) and urban dwellers (88.5%). Similar proportions of women attended high school (30.2%) and college and above (31.8%) followed by those (26.8%) who could read and write. Occupationally, 43% of the participants were housewives followed by government employees (29.4%). Most (57.8%) earned above 1000 Ethiopian Birr (ETB) per month while 19.3% earned less than 500 ETB (1 USD ≈ 20 ETB, 2014 exchange rate) (Table 1).
Table 1

Sociodemographic characteristics of pregnant women attending ANC at Felege Hiwot Referral Hospital, November 2013 to June 2014

Characteristics

Frequency (n)

Percentage (%)

Age categories (years)

 < 20

6

1.6

 20–29

283

73.7

 30–39

88

22.9

 ≥ 40

7

1.8

Marital status

 Single

21

5.5

 Divorced

5

1.3

 Married

358

93.2

Residence

 Rural

44

11.5

 Urban

340

88.5

Educational status

 Illiterate

43

11.2

 Read and write

103

26.8

 High school

116

30.2

 College and above

122

31.8

Occupational status

 Government employee

113

29.4

 Private

86

22.4

 House wife

165

43.0

 Daily laborers

20

5.2

Monthly income (Eth Birr)

 < 500

74

19.3

 500–1000

88

22.9

 > 1000

222

57.8

Seroprevalence of syphilis across socio-demographic variables

Of the total of 384 participants, 10 (2.6%) were seropositive for syphilis. A significant association between syphilis and age categories, marital status and residence of the subjects was observed. Most of the infections were detected among 40 and above years old (28.5%) and divorced women (40%). Three fold higher (6.8%) seroprevalence was found among rural dwelling compared to urban dwelling women (2.1%) (Table 2).
Table 2

Socio-demographic characteristics of pregnant women in relation to their serostatus at Felegehiwot Referral Hospital, November 2013 to June 2014

Characteristics

Total examined

n (%)

Serostatus for T. pallidum

χ2 (df)

p value

COR (CI 95%)

P-value

Positive

n (%)

Negative

n (%)

Age categories (years)

 < 20

6 (1.5)

0 (0)

6 (100)

 

1.00

 

 20–29

283 (73.6)

7 (2.4)

276 (97.6)

19.53

0.02 (0.00, 0.30)

0.004

 30–39

88 (22.9)

1 (1.1)

87 (98.9)

(3)

0.07 (0.01, 0.47)

0.006

 ≥ 40

7 (1.8)

2 (28.5)

5 (71.5)

P = 0.000

0.04 (0.00, 54)

0.015

Marital status

 Single

21 (5.5)

3 (14.3)

18 (85.7)

18.92

0.67 (0.54, 8.19)

0.751

 Divorced

5 (1.3)

2 (40)

3 (60)

(2)

9.77 (2.26, 2.29)

0.002

 Married

358 (93.2)

5 (1.4)

353 (98.6)

P = 0.000

1.00

 

Residence

 Urban

340 (88.5)

7 (2.1)

333 (97.9)

3.47 (1)

1.00

0.079

 Rural

44 (11.5)

3 (6.8)

41 (93.2)

P = 0.052

3.48 (0.86, 13.98)

 

Educational status

 Illiterate

43 (11.2)

4 (9.3)

39 (90.6)

1.11 (3)

1.62 (0.26, 10.09)

0.262

 Read and write

103 (26.8)

3 (2.9)

100 (97.1)

P = 0.774

2.78 (0.37, 20.38)

0.379

 High school

116 (30.2)

2 (1.7)

114 (98.3)

 

1.93 (0.31, 11.99)

0.312

 College and above

122 (31.8)

1 (0.8)

121 (99.1)

 

1.00

 

Occupational status

 Govt. employee

113 (29.4)

1 (0.9)

112 (99.1)

 

1.00

 

 Private

86 (22.3)

3 (3.6)

83 (96.4)

5.91 (3)

0.25 (0.02, 2.41)

0.230

 House wife

165 42.9)

4 (2.4)

161 (97.6)

P = 0.116

0.36 (0.04, 3.25)

0.363

 Daily laborer

20 (5.2)

2 (10)

18 (90)

 

0.08 (0.07, 0.93)

0.044

Family monthly income (Eth Birr)

 < 500

74 (19.3)

3 (4.1)

71 (95.9)

3.29 (2)

0.32 (0.64–1.64)

0.174

 500–1000

88 (22.9)

3 (3.4)

85 (96.6)

P = 0.193

0.28 (0.63, 1.13)

0.108

 > 1000

222 (57.8)

4 (1.8)

218 (98.2)

 

1.00

 

Medical history, sexual behavior and awareness of subjects

About 43.5%, 30.7% and 25.8% of the women had one, two and more than two pregnancies, respectively. A quarter (24.7%) of participants reported history of abortion and while 5.7% encountered stillbirths. Thirty-nine (10.2%) of the women were in their first, (35.4%) second and (54.4%) third trimesters of their pregnancies. More than 90% and 68.2% of the participants had no any previous history of STD and multi-sexual exposure, respectively. Majority (78.4%) of study subjects had awareness towards sexual transmission of syphilis while almost three-fourth (73.0%) did not know transplacental transmission of the disease. Likewise, majority (66.9%) of subjects did not clearly identify the symptoms of syphilis while the rest (33.1%) clearly knew the symptoms of the disease. About 85% of the subjects knew that STDs could be prevented through the use of condom. Majority (74.1%) of the participants’ partners did not use condom during sexual activity (Table 3).
Table 3

Syphilis infection in relation to clinical history, sexual behavior, and awareness of pregnant women about the disease

Characteristics

Total examined

n (%)

Serostatus

X2 (df)

P-value

COR (CI 95%)

P-value

Positive

n (%)

Negative

n (%)

Parity

 Primigravidae

167 (43.5)

3 (1.8)

164 (98.2)

5.58 (2)

1.00

 

 Bigravidae

118 (30.7)

5 (4.2)

113 (95.8)

P = 0.061

1.12 (0.18,6.86)

0.897

 Multigravidae

99 (25.8)

2 (2.0)

97 (98.0)

 

0.46 (0.08,2.45)

0.368

Gestational period (stage)

 1st trimester

39 (10.2)

3 (10.3)

36 (89.7)

10.1 (2)

1.00

 

 2nd trimester

136 (35.4)

2 (1.5)

134 (98.5)

P = 0.006

5.58 (0.89, 34.68)

0.065

 3rd trimester

209 (54.4)

5 (1.9)

205 (98.1)

 

3.40 (0.77,14.85)

0.104

Stillbirths

 Yes

95 (24.7)

4 (4.2)

91 (95.8)

1.28 (1)

0.48 (0.13,1.74)

0.267

 No

289 (75.3)

6 (2.0)

283 (98.0)

P = 0.257

1.00

 

History of abortion

 Yes

22 (5.7)

2 (9.0)

20 (91.0)

3.82 (1)

4.42 (0.88,22.21)

0.071

 No

362 (94.3)

8 (2.2)

354 (97.8)

P = 0.049

1.00

 

History of any STDs

 Yes

34 (8.9)

2 (5.9)

32 (94.1)

1.58 (1)

2.67 (0.54,13.11)

0.226

 No

350 (91.4)

8 (2.3)

342 (97.7)

P = 0.209

1.00

 

Multi-sexual exposure

 Yes

122 (31.8)

7 (5.7)

115 (94.3)

3.95 (1)

5.25 (1.33, 20.68)

0.018

 No

263 (68.2)

3 (1.1)

260 (98.9)

P = 0.009

1.00

 

Condom use

 Yes

99 (25.9)

2 (2.0)

97 (98.0)

0.17 (1)

1.00

0.673

 No

285 (74.1)

8 (2.7)

277 (97.2)

P = 0.672

0.71 (0.14, 3.42)

 

Reason not to use condom

 Partner objection

39 (13.7%)

2 (5.1%)

37 (94.9%)

1.99 (4)

2.19 (0.35, 13.65)

0.386

P = 0.737

 Dislike using condom

70 (24.56%)

2 (2.9%)

68 (97.1%)

 

1.19 (0.19, 7. 33)

0.846

 Ashamed to ask my partner

51 (17.89%)

2 (4%)

49 (96%)

 

1.65 (0.26, 10.24)

0.581

 Faithful to my partner

125 (43.85%)

3 (2.4%)

122 (97.6%)

 

1

 

Knowledge of sexual transmission

 Yes

301 (78.4)

7 (2.3)

294 (97.7)

0.42 (1)

1.00

0.517

 No

83 (21.6)

3 (3.6)

80 (96.4)

P = 0.514

0.63 (0.16, 2.51)

 

Knowledge of transplacental transmission

 Yes

104 (27.0)

3 (2.9)

101 (97.1)

0.04 (1)

1.00

0.738

 No

280 (73.0)

7 (2.5)

273 (97.5)

P = 0.833

1.30 (0.27, 6.31)

 

Knowledge about symptoms

 Yes

127 (33.1)

3 (2.4)

124 (97.6)

0.040 (1)

1.00

0.834

 No

257 (66.9)

7 (2.7)

250 (97.3)

P = 0.834

1.15 (0.29,4.55)

 

Knowledge of prevention of STI through condom use

 Yes

326 (84.9)

6 (1.8)

320 (98.2)

4.96 (1)

1.00

0.038

 No

58 (15.1)

4 (6.9)

54 (93.1)

P = 0.833

3.95 (1.07,14.46)

 

Statistically significant association was observed between syphilis and gestational period, multi-sexual exposure and previous history of still birth. The highest (10.3%) and the lowest (1.5%) prevalence of syphilis were found in pregnant women who were in their first and second trimesters. Participants who had multi-sexual exposure were more (5.7%) infected than unexposed ones (1.1%). In contrast, parity, history of STDs, habit of condom use and awareness of women towards transmission and prevention were not associated with syphilis.

Univariate logistic regression analysis of potential risk factors

Divorced women were 9.77 times more likely to be infected with syphilis than married ones. Similarly, the odds of syphilis were 3.48 times higher among rural residing pregnant women compared to urban dwellers. However, no associations were detected between syphilis and age, occupation, educational status, and monthly income (Table 2).

Pregnant women who were in their second and third trimesters were 5.85 and 3.40 times more likely infected with syphilis compared with those in their first trimester. Furthermore, the risk of T. pallidum infection was 4.42 and 2.67 times higher among those who had previous history of abortion and STIs, respectively. Pregnant women who had previous history of multi-sexual exposure were at 5.25 folds of increased risk of getting the infection compared to those women who had no exposure at all. Likewise, nearly fourfolds of risk of the disease were observed among women who had no knowledge of prevention of STDs through condom use compared to those who had the awareness. However, no significant association was observed between syphilis and the risk factors considered like parity, history of stillbirth, habit of condom use and knowledge of the study subjects toward sexual and transplacental transmission and symptoms of this disease (Table 3).

Discussion

The seroprevalence of syphilis among pregnant women in current study was 2.6%. This is consistent with reports of two hospital based studies in Ethiopia [15, 16]. However, it is much higher than syphilis sero-positivity reported among pregnant women in Nigeria (0.3%) [11] and in Tanzania (0.5%) [17]. It is also higher than findings from India (0.36%) [18] and China (0.39%) [19]. Compared to similar studies, it is lower than prevalence of 4.3%, 5.0%, 5.8% and 7.3% reported from Botswana [20], Malawi [21], the Niger Delta, Nigeria [22] and Tanzania [23], respectively. These discrepancies in the seroprevalence of syphilis among different populations within and outside Ethiopia might be a reflection of variations in sexual practice and behavior of the communities, awareness about syphilis and difference in access to treatment of STDs, cultural practices, and also differences in the laboratory techniques employed in detecting T. pallidum infection.

In Several epidemiological studies found significant association between risk of syphilis and educational status, where study subjects with no education or less educational attainment were at higher risk of getting syphilis [24, 25, 26, 27]. Contrary to this, in our study we could not find any association between educational status and T. pallidum seropositivity. Nevertheless, the significance of education toward avoidance of the potential risk factors cannot be ruled out.

It was found that divorced pregnant women were ten times more likely to be infected with syphilis than married women. This might be due to the tendency of divorced women to have more sexual partners. On the contrary, reports from southern [26] and central [28] Ethiopia showed no association between marital status and syphilis.

In this study, no statistically significant association was found between parity and syphilis. This is in conformity with the report of Onwuezobe et al. [29]. However, a study done at Harare Maternity Hospital reported significant increase in the risk of syphilis as the parity increased [30].

Being at the third trimester was significantly associated with the syphilis and it was shown that women at this stage of pregnancy were three times more likely to get the infection compared to those at first trimester of pregnancy. This finding could be attributed to a possible common practice where most pregnant women visit ANC later in their pregnancies.

In our study, the risk of syphilis was greater in women with previous history of abortion and other STDs. This is in line with Zhou et al. [27] and Macêdo et al. [31] who reported significant association between syphilis and prior history of induced abortion and other STDs.

The likelihood of syphilis was almost two times higher among women living in rural setting as compared to their urban dwelling counterparts. This could be due to low level of awareness of women and limited access to mass media and social networks in rural areas. Contrary to the current finding, Assefa [15] reported a relatively higher rate of this disease among urban pregnant women.

Pregnant women who had previous history of multi-sexual exposure were six times more likely to be infected with syphilis than unexposed ones. This is in agreement with the reports of Eticha et al. [28], Moges [32] and Sule [33] who noted increased odds of syphilis among women with many sexual partners as compared to those with one sexual partner.

In conclusion, the seroprevalence of syphilis in this study was relatively lower than previous studies in Ethiopia. This might be due to preventive interventions taken and improved surveillances. Prevalence of syphilis was strongly associated with variables like rural residence, divorced marital status, and history multiple sexual exposure of the participants. So, raising the awareness of the community towards safe sex practice is still important in the reduction of the prevalence of the disease not only in pregnant women but also in general population.

Limitation

Since this is a hospital based cross-sectional study, the reported prevalence of syphilis might not reflect the actual burden of the disease at community level. The study might be susceptible to responder recall and interviewer bias regarding the risk factors.

Notes

Authors’ contributions

AM and EN conceived and designed the study. AM and KT collected samples and performed the laboratory works. EN and KT checked and analyzed the data. AM wrote the manuscript. EN and KT edited the manuscript. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to thank the Research and Community Service Office of the College of Science, Bahir Dar University for the financial support, the study participants for their involvement in this study and the laboratory technicians, nurses and doctors of Bahir Felege Hiwot Referral Hospital for their assistance during blood sample and data collection.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The socio-demographic, behavioural parameters and clinical data of the subjects enrolled in the study are anonymously collected in a dataset. The readers may contact the corresponding author to access these data.

Consent to publish

Not applicable.

Ethics approval and consent to participate

The study protocol was reviewed and approved by the Ethical Review Committee of Postgraduate, Research and Community Service office of College of Science, Bahir Dar University, Ethiopia. Written informed consent was obtained from all participants before their enrolment into the study. Then, interviewer administered questionnaire to gather information on socioeconomic, behavioral characteristics and clinical parameters of the pregnant women and blood samples were collected for serological analysis. Subject confidentiality and privacy were protected by ensuring that no names appeared on any part of the report. Pregnant women who were found to be syphilis seropositive were advised to attend at STI clinics with their partners for treatment.

Funding

This research was partly supported by the Research and Community Service office of College of Science, Bahir Dar University, Ethiopia with identification number BDU/RCS/Sc 32/2007.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.
    Peeling RW, Hook EW. The pathogenesis of syphilis: the Great Mimicker, revisited. J Pathol. 2006;208:224–32.CrossRefGoogle Scholar
  2. 2.
    Miller BA, Hicks CB. Syphilis and HIV: the intersection of two epidemics. 2010. http://www.jwatch.org/ac201009030000001/2010/09/03/syphilis-and-hiv-intersectiontwo-epidemics. Accessed 11 Oct 2014.
  3. 3.
    Camerona CE, Lukehartb SA. Current status of syphilis vaccine development: need, challenges, prospects. Vaccine. 2014;32(14):1602–9.CrossRefGoogle Scholar
  4. 4.
    World Health Organization. The Global elimination of congenital syphilis: rationale and strategy for action. Geneva: World Health Organization; 2007.Google Scholar
  5. 5.
    Stamm LV. Global challenge of antibiotic-resistant Treponema pallidum. Antimicrob Agents Ch. 2010;54:583–9.CrossRefGoogle Scholar
  6. 6.
    World Health Organization. Prevalence and incidence of selected sexually transmitted infections Chlamydia trachomatis, Neisseria gonorrhoeae, syphilis and Trichomonas vaginalis: methods and results used by WHO to generate 2005 estimates. Geneva: World Health Organization; 2011.Google Scholar
  7. 7.
    Schmid G. Economic and programmatic aspects of congenital syphilis prevention. Bull World Health Organ. 2004;82(6):402–9.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Rydzak CE, Goldie SJ. Cost-effectiveness of rapid point-of-care prenatal syphilis screening in sub-Saharan Africa. Sex Transm Dis. 2008;35:775–84.CrossRefGoogle Scholar
  9. 9.
    Karumudi UR, Augenbraun M. Syphilis and HIV: a dangerous duo. Expert Rev Anti Infect Ther. 2005;3:825–31.CrossRefGoogle Scholar
  10. 10.
    Mullick S, Watson-Jones D, Beksinska M, Mabey D. Sexually transmitted infections in pregnancy: prevalence, impact on pregnancy outcomes, and approach to treatment in developing countries. Sex Transm Infect. 2005;81:294–302.CrossRefGoogle Scholar
  11. 11.
    Ogiogwa JI, Akingbade OA, Aboderin BW, Okerentugba PO, Innocent-Adiele HC, Onoh CC, et al. Prevalence of Treponema pallidum in serum of pregnant women in Abeokuta, Ogun State, Nigeria. Nat Sci. 2012;10:91–4.Google Scholar
  12. 12.
    Todd J, Munguti K, Grosskurth H, Mngara J, Changalucha J, Mayaud P, et al. Risk factors for active syphilis and TPHA seroconversion in a rural African population. Sex Transm Infect. 2001;77(1):37–45.CrossRefGoogle Scholar
  13. 13.
    BoFED. Population Affairs Reports of Bureau of finance and economic development (BoFED) of Amhara National Regional State (ANRS). Bahir Dar: BoFED; 2014.Google Scholar
  14. 14.
    Naing L, Winn T, Rusil BN. Practical issues in calculating sample size for prevalence studies. Archel Orphanet Sci. 2006;1:9–14.Google Scholar
  15. 15.
    Assefa A. A three year retrospective study on seroprevalence of syphilis among pregnant women at Gondar University Teaching Hospital, Ethiopia. Afr Health Sci. 2014;14:119–24.CrossRefGoogle Scholar
  16. 16.
    Endris M, Deressa T, Belyhun Y, Moges F. Seroprevalence of syphilis and human immunodeficiency virus infections among pregnant women who attend the University of Gondar teaching hospital, Northwest Ethiopia: a cross sectional study. BMC Infect Dis. 2015;15:111.CrossRefGoogle Scholar
  17. 17.
    Yahya-Malima IK, Evjen-Olsen B, Matee IM, Fylkesnes K, Haarr L. HIV-1, HSV-2 and syphilis among pregnant women in a rural area of Tanzania: prevalence and risk factors. BMC Infect Dis. 2008;8:75.CrossRefGoogle Scholar
  18. 18.
    Nair N, Urhekar AD, Pachpute S, Srivastava A. Incidence of Syphilis among pregnant women attending a tertiary care hospital in Navi Mumbai, India. Int J Curr Microbiol. 2013;2:79–84.Google Scholar
  19. 19.
    Yang L, Tucker DJ, Liu FY, Ren XQ, Hong X, Wang C, et al. Syphilis screening among 27,150 pregnant women in South Chinese rural areas using point-of-care tests. PLoS. 2013;8:e72149.CrossRefGoogle Scholar
  20. 20.
    Creek TL, Thuku H, Kolou B, Rahman M, Kilmarx PH. Declining syphilis prevalence among pregnant women in northern Botswana: an encouraging sign for the HIV epidemic? Sex Transm Infect. 2005;81:453–5.CrossRefGoogle Scholar
  21. 21.
    Kwiek JJ, Mwapasa V, Alker AP, Muula AS, Misiri HE, Molyneux ME, et al. Socio-demographic characteristics associated with HIV and syphilis seroreactivity among pregnant women in Blantyre, Malawi, 2000–2004. Malawi Med J. 2008;20:80–5.CrossRefGoogle Scholar
  22. 22.
    Buseri FI, Seiyaboli E, Jeremiah ZA. Surveying infections among pregnant women in Niger Delta. Niger J Glob Infect Dis. 2010;2:202–11.Google Scholar
  23. 23.
    Swai RO, Geofrey RS, Matee MI, Ndayongeje J. Surveillance of HIV and syphilis infections among antenatal clinic attendees in Tanzania-2003/2004. BMC Public Health. 2006;6:1470–2458.CrossRefGoogle Scholar
  24. 24.
    Ruan Y, Luo F, Jia Y, Li X, Li Q, Liang H, et al. Risk factors for syphilis and prevalence of HIV, hepatitis B and C among men who have sex with men in Beijing, China: implications for HIV prevention. AIDS Behav. 2009;13(4):663–70.CrossRefGoogle Scholar
  25. 25.
    Miranda AE, Figueiredo NC, Pinto VM, Page K, Talhari S. Risk factors for syphilis in young women attending a family health program in Vitória, Brazil. An Bras Dermatol. 2012;87(1):76–83.CrossRefGoogle Scholar
  26. 26.
    Shimelis T, Lemma K, Ambachew H, Tadesse E. Syphilis among people with HIV infection in southern Ethiopia: sero-prevalence and risk factors. BMC Infect Dis. 2015;15:189.CrossRefGoogle Scholar
  27. 27.
    Zhou H, Chen X-S, Hong F-C, Pan P, Yang F, Cai Y-M, et al. Risk factors for syphilis infection among pregnant women: results of a case-control study in Shenzhen, China. Sex Transm Infect. 2007;83:476–80.  https://doi.org/10.1136/sti.2007.026187.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Eticha TB, Sisay Z, Alemayehu A, Shimelis T. Seroprevalence of syphilis among HIV-infected individuals in Addis Ababa, Ethiopia: a hospital-based cross-sectional study. BMJ Open. 2013;3:e002566.CrossRefGoogle Scholar
  29. 29.
    Onwuezobe IA, Ochang EA, Umoiyoho A, Bassey EA, Umoffia EM. Prevalence of syphilis seropositivity in antenatal clinic clients in a teaching hospital in South–South region of Nigeria. APJTM. 2011;1:21–3.CrossRefGoogle Scholar
  30. 30.
    Pham L, Woelk GB, Ning Y, Madzime S, Mudzamiri S, Mahomed K, et al. Seroprevalence and risk factors of syphilis infection in pregnant women delivering at Harare Maternity Hospital, Zimbabwe. Cent Afr J Med. 2005;51(3–4):24–30.PubMedGoogle Scholar
  31. 31.
    Macêdo VC, Lira PIC, Frias PG, Romaguera LMD, Caires SFF, Ximenes RAA. Risk factors for syphilis in women: case-control study. Rev Saude Publica. 2017;51:78.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Moges F, Kebede Y, Kassu A. Seroprevalence of HIV, HBV infections and syphilis among street dwellers in Gondar city, northwest Ethiopia. Ethiop J Health Dev. 2006;20:160–5.Google Scholar
  33. 33.
    Sule J. Treponema pallidum specific antibodies among sexually active people. Appl Biosci. 2010;28:1731–5.Google Scholar

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  • Kiros Tareke
    • 1
  • Abaineh Munshea
    • 1
    • 2
    Email author
  • Endalkachew Nibret
    • 1
    • 2
  1. 1.Biology Department, College of ScienceBahir Dar UniversityBahir DarEthiopia
  2. 2.Biotechnology Research InstituteBahir Dar UniversityBahir DarEthiopia

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