Predicting adverse pregnancy outcomes of pregnant mothers with syphilis based on a logistic regression model: a retrospective study

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Predicting adverse pregnancy outcomes of pregnant mothers with syphilis based on a logistic regression model: a retrospective study

https://doi.org/10.21203/rs.3.rs-1747566/v1

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Objective: To assess whether a simple predictive model can be composed of risk factors leading to adverse pregnancy outcomes (APOs) in infants of syphilitic mothers during pregnancy, that can predict the APOs of newborns.

Methods: We conducted a retrospective study of 768 pregnant women with syphilis. They were required to complete a questionnaire. We analyzed the data and divided it into a training set and a test set. In the training set, we screened the predictors, constructed a prediction model and evaluated the prediction performance in the test set.

Results: Compared with the APOs group, pregnant women in the non-APOs group participated in a longer treatment course. Course, time of the first antenatal care, gestation week at syphilis diagnosis, and gestation age at delivery in weeks were independent predictors of APOs, and they were used to establish the nomogram. The AUCs of the nomogram were 0.771 (95% CI, 0.708-0.834) and 0.733 (95% CI, 0.638-0.828) in the training and testing sets, respectively.

Conclusions: Our study investigated the impact of various characteristics of syphilis pregnant women on pregnancy outcomes and established a prediction model of APOs in Suzhou. The incidence of APOs can be reduced by controlling for these risk factors.

Syphilis maternal

Adverse pregnancy outcomes

APOs

Syphilis is a contagious venereal disease caused by the spirochete Treponema pallidum that can infect infants through vertical transmission and may present with lifelong diseases, including irreversible neurological and cardiovascular complications [1] [2]. Most maternal syphilis infections are latent, and mothers with syphilis often do not have awareness of it until they are diagnosed [3]. Previous studies have concluded that untreated infections can lead to adverse pregnancy outcomes (APOs) [4]. Historical and present studies suggest that untreated syphilis or incompletely treated in pregnancy carries a significant risk of stillbirth, prematurity or low birth weight, neonatal death, and congenital syphilis, among others. [5] [6]. It was estimated that the global maternal syphilis prevalence was 0.69% in 2016, causing a substantial public health burden and cost to families [7]. However, APOs are preventable through prenatal syphilis screening, appropriate pregnancy treatment, and other health interventions [8] [9]. Located in the middle of the Yangtze River Delta, Suzhou is famous for its national high-tech industrial base. The population of Suzhou is 10.72 million, of which 50% are transient. In 2018, the total number of pregnant women and live births in Suzhou were 111488 and 112523, respectively[10]. The city has a large floating population and migrant workers, a demographic structure that is more common in some relatively developed cities in China. Therefore, the sample from this city is representative of maternal and neonatal health in cities with similar levels of economic development.

Only a few studies have reported on the prevalence of maternal syphilis in localized areas of China, focusing mainly on the incidence of congenital syphilis, rather than APOs. Previous studies have shown that APOs caused by syphilis are avoidable. Women who were screened in the first two trimesters of their pregnancy and received adequate treatment had a reduced incidence of congenital syphilis and were more likely to have a healthy infant[11] [12] [13]. Untreated or inadequately treated maternal syphilis is associated with an increased risk of adverse pregnancy outcomes, including early fetal deaths, stillbirths, neonatal death, preterm birth, low birth weight (LBW), and congenital syphilis (CS)[14]. The study aimed to investigate the influence of some maternal characteristics during pregnancy on APOs. [15]. The findings of this study could be useful in guiding maternal and child public health policies in this region.

2.1 Participants

In this retrospective study, the multicentered clinical data of pregnant women with syphilis and their fetuses were obtained from the outpatient clinic of maternal and child health care institutions in Suzhou, Jiangsu Province, China. All syphilis-infected pregnant women with ages 14 to 45 who delivered ≥28 gestational weeks were registered between January 2018 and December 2020 and were enrolled, regardless of their birth outcomes. The Chinese government provides comprehensive syphilis intervention services for all pregnant women free of charge. These services included syphilis counseling and testing at the first antenatal care, treatment for positive cases during pregnancy, follow-up service for exposed infants until they were diagnosed or excluded CS, etc. This study was approved by the Ethics committee of The Affiliated Infectious Diseases Hospital of Soochow University（No.2019002）,and has been performed in accordance with the Declaration of Helsinki. All infected mothers were required to complete a routine questionnaire upon receiving syphilis screening and testing at their first antenatal care or delivery. Informed consent was obtained from syphilis-infected mothers. Prenatal syphilis screening and testing processes followed the guidelines and regulations of the integrated National Preventing Mother to Child Transmission Program of HIV, Syphilis, and Hepatitis B. In the final database, only mothers and infant numbers were listed. All personal information was kept confidential.

2.2 Definitions

The adverse pregnancy outcomes involved in this study included stillbirth, preterm birth, low birth weight (LBW), congenital disabilities, asphyxia, pneumonia, and neonatal CS. Gestational age was based on the interval between the date of the last menstrual period and the date of delivery. Preterm delivery was defined as delivery before 37 completed weeks of gestation. LBW was described as a birth weight of less than 2500 g. The diagnostic criteria of neonatal CS in the study referred to Dou L et al[16].

2.3 Data analysis

Relationships between the fetus with APOS and without APOs were assessed with the χ² test or Fisher’s exact test as appropriate. We randomly divide all samples into a training set (70%) and a test set (30%) according to the random number table. The univariable screening was performed using logistic regression with an inclusion level of 0.05. Then multivariable regression analysis was performed for the statistically significant variables. Then the odds ratios (ORs) and their 95% confidence intervals (CIs) of the factors associated with APOs were estimated. Nomogram, a predictive device, was constructed to predict the probability of outcomes and visualize the results. Next, we evaluated the predictive power of the constructed models in the training and test sets: receiver operating curves, calibration curves, and decision curves were used, respectively. All analyses were performed in R software (version 3.5.3), and the significance level was set to 0.05.

3.1 Basic information on the distribution of the participants

During the observation period from January 2018 to December 2020, 786 pregnant women with syphilis were seen in the outpatient departments of hospitals within the Suzhou metropolitan area. The characteristics of pregnant women with syphilis are shown in Table 1. Their average age was 29.51 ± 5.25 years, and they received an average of 1.54 ± 0.80 courses of treatment. The median gestational age at which they were diagnosed with syphilis was 15 weeks. The majority of these women were married, accounting for 90.9% (722) of the total, with 7.3% (57) and 0.9% (7) being unmarried and divorced, respectively. Infected women of Han ethnicity accounted for 94.4% (742), and only about 17.1% (128) percent have any tertiary education at university or above. Of these, 50.6% (398) had a history of syphilis infection, and 71.2% had a history of APOs with their child born in the past. See Table 1 for more details.

3.2 Comparison of maternal characteristics between newborns with APOs and newborns without APOs

The characteristics of syphilis pregnant women between the newborns with APOs and newborns without APOs are shown in Table 2. Women in the non-APOs group generally participated in a longer treatment course than women in the APOs group. Significant differences in marital status (P= 0.003) and treponema pallidum particle agglutination (TPPA) titer (P=0.03) were observed between the two groups. And more people in the non-APOs group had a history of syphilis infection than in the APOs group (P=0.02). In addition, compared with women in the non-APOs group, those in the APOs group had a younger gestational age at delivery in weeks. More details are provided in Table 2.

3.3 Prediction model analysis of APOS

Univariable logistic regression analysis was used on 20 variables to find significant predictors. Then, it demonstrated that course, time of the first antenatal care, gestation week at syphilis diagnosis, and gestation age at delivery in weeks were potential independent predictors of APOs risk. Further multivariable analysis indicated that these four predictors are valid. The logistic regression results for these four predictors are shown in Table 3.

The predictors are applied to a model that is randomly divided into a training set and a testing set. Four independent predictors were used to establish a nomogram (Fig. 1), and the points of each variable are shown in Table 4. The area under the curve (AUC) of our nomogram was 0.771 (95% CI, 0.708-0.834) in the training set (Fig. 2a), showing good accuracy for predicting APOs. The calibration curves (Fig. 2b) indicate a high degree of agreement between the predictions of the nomogram graphs and actual observations. Moreover, decision curve analysis (DCA) (Fig. 2c) demonstrated that using the nomogram to predict APOs performs well.

The testing set included 235 pregnant women. Put the predictors into the testing set, and the model performs well. In the testing set, the AUC of the nomogram was 0.733 (95% CI, 0.708-0.834) (Fig. 2d), and the calibration curves (Fig. 2e) showed good agreement between the predicted and actual probability of APOs occurrence. Additionally, DCA demonstrated that using the nomogram to predict APOs has a net benefit at all thresholds (Fig. 2f).

The present study investigated the relationship between APOS and syphilitic mothers and constructed a simple predictive model. Our study showed several characteristics among pregnant women regarding treatment status were distributed significantly differently, including treatment course, history of syphilis infections, marital status, TPPA titer, and gestational age at delivery in weeks. Studies regarding the influence of maternal syphilis treatment on pregnancy outcomes found that the above factors were associated with an increased risk of a series of adverse pregnancy outcomes. Therefore, some of them become our predictors for the prediction model of APOs and help us construct the model. Using this model, it is possible to analyse the risk of APOs in pregnant women with syphilis and to provide guidance for them.

Our study showed that course, time to diagnosis, maternal clinical characteristics, marital status, and history of syphilis infection were associated with APOs. A multivariate regression study showed that a higher titre was a risk factor for APOs, and being married was a protective factor[17]. Another study in Suzhou showed that with every 2-fold increase in TPPA titer, the odds of congenital syphilis increase by 60%[18]. Unlike other studies[19], age was not a risk factor for APO, presumably related to sample size.

Based on four predictors, our model was established as a tool that can predict the APOs risk of syphilis-infected women. We found that pregnant women with syphilis who had adverse pregnancy outcomes had fewer treatment sessions. Similar results have been described in previous studies, and inadequate treatment and treatment initiated in late pregnancy remained risk factors for APOs [3] [20] [19]. A Retrospective Cohort Study in China compared different treatments and concluded that China-recommended therapy, two courses of penicillin treatment, might have a large in reducing multiple APOs [21].

The time of the first antenatal care and gestation week at syphilis diagnosis was also associated with pregnancy outcomes, consistent with other studies[22] [23]. Early antenatal care can facilitate early detection of maternal syphilis and prompt treatment for those with positive tests[24]. Estimated by a hazards model: each 1-week delay in the start of prenatal care may increase the risk of congenital syphilis by approximately 10%.[25]. Factors that contribute to the occurrence of APOs are related to the gestational age at the time of diagnosis and may be related to the management received after diagnosis. A multivariable logistic regression showed that syphilis-infected mothers diagnosed at >36 weeks' gestational age were approximately 25 times more likely to deliver an infant with congenital syphilis compared to women diagnosed at ≤12 weeks' gestational age [18].

The full gestational age at delivery in weeks is a crucial predictor of the occurrence of APOs. This factor was hardly discussed in the same type of studies. A cohort study in Norway [26] showed that the risk of APOs was highest at 37 and 42 weeks and lowest at 39 weeks. Consistent with our findings.

In China, all pregnant women could receive two courses of treatment for free as soon as a diagnosis of syphilis infection was made during pregnancy [27]. However, some patients do not receive standardized anti-syphilis treatment because of weak reproductive health knowledge or unfamiliarity with the prenatal care system, and fear of discrimination by their spouses or medical personnel [28] [29]. Future efforts should include health promotion and improving treatment adherence. It is recommended to start prenatal care as early as possible, which means syphilis can be diagnosed and treated as soon as possible.

A review evaluating the optimal timing of prenatal interventions to prevent mother-to-child transmission of syphilis and APOs suggests that women who received interventions (including screening and treatment) in the first and second trimesters of pregnancy have a lower incidence of adverse outcomes compared to those in the late stages of the pregnancy[13]. The risk of trans-placental infection is 60-80% and the likelihood of infection increases in the second half of pregnancy[9].Infants of women who first sought antenatal care in the third trimester or at delivery often already have congenital syphilis[30].

Studies have been conducted to analyse risk factors for the development of adverse outcomes in pregnant women with syphilis. Our study builds on this by designing a model that quantifies the risk. Based on the estimated risk results, obstetricians can provide treatment recommendations to their patients.

Our study has the following limitations. First, we lack the support of other databases for external validation of model accuracy. Second, only women who delivered ≥28 gestational weeks were included in the study. Hence, some adverse birth outcomes, including early fetal loss and miscarriage, might be underestimated. In a follow-up study, we plan to add comparisons with other data to refine our model.

Our study investigated the impact of various characteristics of syphilis pregnant women on pregnancy outcomes and established a prediction model of APOs in Suzhou, Jiangsu Province, China. This study suggested that gestational age at delivery in weeks plays a crucial role in predicting adverse pregnancy outcomes. We should strive to ensure that pregnant women with syphilis receive appropriate treatment during pregnancy and implement a policy of early screening and timely diagnosis for all syphilis patients.

APO: Adverse pregnancy outcomes; TPPA: Treponema pallidum particle agglutination; AUC: area under the curve; DCA: decision curve analysis

7. Acknowledgments

This study was approved by the Ethics committee of The Affiliated Infectious Diseases Hospital of Soochow University（No.2019002）. All infected mothers were required to complete a routine questionnaire upon receiving syphilis screening and testing at their first antenatal care or delivery. Informed consent was obtained from syphilis-infected mothers. Prenatal syphilis screening and testing processes followed the guidelines and regulations of the integrated National Preventing Mother to Child Transmission Program of HIV, Syphilis, and Hepatitis B. In the final database, only mothers and infant numbers were listed. All personal information was kept confidential. This work was supported by the Science and Technology Project in Suzhou (SS2019043). The authors had complete control over the design, conduct, and analysis of the study and the decision to submit the manuscript for publication.

8.Competing interests

The authors declare that there are no conflicts of interest.

9.Data Availability Statement

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

10.Authors’ Contributions

Zhang, Y. W., Liu, M.Y, Yu, X.H., Liu. X and Yana Ma made substantial contributions to the design of the work. Zhang, Y. W. and Liu, M.Y analysed the data and rafted the manuscript. He. X.Y. collected the data. Yu, X.H. and He. X.Y. designed the research. Yu, X.H. and Wang. D. analysed the data. Liu. X. and Ma, Y. N. performed the research. All authors have read and approved the final manuscript.

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Table 1 Characteristics of syphilis pregnant women （N=786）

	Mean	SD	Median	IQR	N	%
Course	1.54	0.80
Age	29.51	5.25
Time of the first antenatal care			13.00	[12.00, 16.00]
Gestation week at syphilis diagnosis			15.00	[13.00,22.50]
Gestation age at delivery in weeks			39.00	[38.00,40.00]
TPPA titer			2.00	[1.00, 4.00]
Marital status
Unmarried					57	7.3
Married					722	91.9
Divorced					7	0.9
Ethnicity
Han					742	94.4
Others					44	5.6
Education
Illiterate / semi-literate					6	0.8
Primary school					48	6.4
Junior high school					565	75.6
University or college					127	17.0
Master and above					1	0.1
History of syphilis infections
Yes					398	50.6
No					388	49.4
History of APOs
Yes					560	71.2
No					226	28.8

Note: Junior high school including junior high school, vocational high school, technical school, etc.

APOs: adverse pregnancy outcomes.

RPR: rapid plasma regain.

TRUST: toluidine red unheated serum test.

TPPA: treponema pallidum particle agglutination.

Table 2 Comparison of maternal sociodemographic characteristics and syphilis condition between newborns with APOs and newborns without APOs

	Without APOs 648	With APOs 138	P value
	Mean (SD)/M(IQR)/N (%)	Mean (SD)/M(IQR)/N (%)	P value
Course	1.59(0.78)	1.30(0.87)	<0.001
Age	29.51(5.12)	29.49(5.81)	0.96
Gravidity	3.00[2.00, 4.00]	3.00[2.00, 4.00]	0.72
Parity	1.00[0.00, 1.00]	1.00[0.00, 1.00]	0.76
Number of children present	1.00[0.00, 1.00]	0.00[0.00, 1.00]	0.73
Time of the first antenatal care	13.00[12.00, 16.00]	13.00[11.25, 23.25]	0.13
Gestation week at syphilis diagnosis	15.00[13.00, 21.00]	16.00[13.00, 31.00]	0.054
Gestation age at delivery in weeks	39.00[38.00, 40.00]	37.00[35.00, 39.00]	<0.001
RPR/TRUST Titer	2.00[1.00, 4.00]	2.00[1.00, 7.00]	0.06
TPPA titer	2.00[1.00, 4.00]	2.00[1.00, 8.00]	0.03
RPR/TRUST Titer of newborns	2.00[1.00, 2.00]	2.00[1.00, 6.00]	0.02
Ethnicity			0.93
Han	611 (94.3)	131(94.9)
Others	37 (5.7)	7(5.1)
Education			0.95
Illiterate / semi-literate	5(0.8)	1(0.8)
Primary school	40(6.5)	8(6.1)
Junior high school	462(7.5.1)	103(78.0)
University or college	107(17.4)	20(15.2)
Master and above	1(0.2)	0(0.0)
Employment			0.07
Farmer	143(25.6)	23(18.0)
Business	48(8.6)	7(5.5)
Institution	13(2.3)	6(4.7)
Others	354(63.4)	92(71.9)
Marital status			0.003
Unmarried	38(5.9)	19(13.8)
Married	603(93.1)	119(86.2)
Divorced	7(1.1)	0(0.0)
History of APOs			0.56
Yes	465(71.8)	43(31.2)
No	183(28.2)	95(68.8)
History of syphilis infections			0.02
Yes	341(52.6)	57(41.3)
No	307(47.4)	81(58.7)
Period of maternal syphilis detection			<0.001
Gestation	591(91.2)	108(78.3)
At delivery/postpartum	57(8.8)	30(21.7)
Mode of delivery			0.55
Caesarean section	331(51.1)	75(54.3)
Normal or assisted delivery	317(48.9)	63(45.7)
Number of childbirth			0.053
Singleton	636(98.1)	131(94.9)
Twins	12(1.9)	7(5.1)
Sex of the fetus			0.15
Male	347(53.5)	60(46.2)
Female	301(46.5)	70(53.8)
Pre-treatment			0.88
Positive	506(79.4)	107(80.5)
Negative	131(20.6)	26(19.5)
RPR/TRUST			0.87
Positive	259(42.5)	47(43.5)
Negative	350(57.5)	60(56.1)
TPPA			0.56
Positive	535(98.5)	95(95.0)
Negative	8(1.5)	5(5.0)
Newborns with preventive treatment			0.44
Yes	410(63.3)	77(59.2)
No	238(36.7)	53(40.8)

Note: Junior high school including junior high school, vocational high school, technical school, etc.

Table 3 Univariable and multivarible factors logistic regression analysis of APOs

	Univariable logistic regression analysis				Multivariable logistic regression analysis
	OR	95%CI		P	OR	95%CI		P
Course	0.572	0.439	0.744	<0.001	0.695	0.487	0.992	0.04
Time of the first antenatal care	1.019	1.008	1.03	<0.001	1.011	0.994	1.029	0.20
Gestation week at syphilis diagnosis	1.022	1	1.044	0.05	0.975	0.942	1.009	0.15
Gestation age at delivery in weeks	0.566	0.49	0.653	<0.001	0.576	0.497	0.668	<0.001

Table4 Multivariable logistic regression models for prediction of APOs

	BETA	SE	Z	estimate	P value
Course	-0.36	0.18	-2.01	0.695 (0.487,0.992)	0.04
Time of the first antenatal care	0.01	0.01	1.29	1.011 (0.994,1.029)	0.20
Gestation week at syphilis diagnosis	-0.03	0.02	-1.44	0.975 (0.942,1.009)	0.15
Gestation age at delivery in weeks	-0.55	0.08	-7.28	0.576 (0.497,0.668)	<0.001

No competing interests reported.

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Predicting adverse pregnancy outcomes of pregnant mothers with syphilis based on a logistic regression model: a retrospective study

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