1. Introduction
Syphilis is a chronic infectious disease, commonly caused in humans by
Treponema pallidum (TP) infection. It principally spreads through sexual contact, vertical transmission, and blood transmission [
1,
2]. Early signs of syphilis usually manifest as genital and skin mucous membrane damage, while late syphilis can involve the bones, nerves, and cardiovascular system. [
3,
4]. According to the 2021 WHO Global Progress Report on HIV, Viral Hepatitis and Sexually Transmitted Diseases, an estimated 7.1 million new cases of syphilis (95% UI: 3.8–10.3 million) were reported worldwide in 2020, an increase of nearly 800,000 from over 6.3 million in 2016 [
5,
6]. As one of the class B notifiable infectious diseases in China, the reported incidence of syphilis in 2020 was the third highest after viral hepatitis and tuberculosis [
7]. Thus, syphilis is still one of the most severe sexually transmitted infection, warranting global prevention and control since it can cause serious harm to human health.
About 80% of epidemiological data have spatial attributes [
8]; thus, analyzing the spatiotemporal distribution characteristics of syphilis incidence and further exploring the meteorological or socio-economic driver factors associated with the spatiotemporal heterogeneity of syphilis incidence can promote the development of effective responses for high-risk areas [
9,
10,
11,
12]. Liu et al. [
13] suggests that the rapid spread of syphilis may be the result of a combination of biological and social factors. From the perspective of geographical distribution of syphilis incidence, the affected regions in China gradually expanded from southeast coastal areas with relatively rapid economic development regions to north and southwestern inland areas [
14,
15,
16]. From the perspective of associated meteorological or socio-economic factors, previous studies have shown inconsistent results concerning associated factors of syphilis incidence. For example, Smock et al. [
17] found that syphilis incidence was higher in poverty-level groupings. However, Read et al. [
18] showed that economically developed areas had a higher risk of syphilis. Thus, syphilis incidence in different regions showed a significant spatial discrepancy and conflicting results regarding the potential associated socio-economic or meteorological factors.
Identifying key areas of syphilis incidence based on spatiotemporal distribution studies, and combining evidence of potential meteorological or socio-economic drivers to adjust syphilis prevention strategies and allocate health resources is of great significance for effective syphilis prevention and control. Current spatial econometric methods are widely used in public health and health policy evaluation [
19,
20,
21,
22]. Tang et al. [
11] applied a spatial panel data model to explore the relationship between socio-demographic factors, socio-economic factors, and the incidence of primary and secondary syphilis in Guangdong China after controlling for spatial effects. Salway et al. [
23] described the spatial-temporal epidemiology of infectious syphilis and identified the associations between neighborhood-level factors and rates of syphilis in British Columbia, Canada. Understanding the potential drivers of the incidence of syphilis has developed from traditional epidemiology to spatial epidemiology; however, there are still few related studies on its potential influencing factors.
Ningxia Hui Autonomous Region (referred as “Ningxia”), located in northwest China, is an economically underdeveloped region, bordering the Gansu and Shaanxi provinces. According to a report by the Ningxia Center for Disease Control and Prevention, syphilis remains a growing and resurging infectious disease. Existing evidence showed that socio-economic and health-resource factors may affect the spatial distribution of syphilis [
11]; however, there are very few result related to the association between these factors and spatial heterogeneity of syphilis in Ningxia. To fill this gap, we used spatial autocorrelation and scan analyses to investigate the spatiotemporal distribution characteristics of syphilis in Ningxia, based on the number of reported syphilis cases in 22 administrative areas in the Ningxia region from 2004 to 2017. We then constructed a spatial panel regression model to explore the potential socio-economic, health-resource factors, and meteorological factors that influence the distribution of syphilis incidence. These results may provide a theoretical basis for precisely adjusting syphilis prevention and control in high-risk regions of Ningxia.
4. Discussion
In order to effectively strengthen syphilis prevention and control, the 59th World Health Assembly adopted the Prevention and Control of Sexually Transmitted Infections: Draft Global Strategy [
35] in 2006, and in 2010 China formulated the China Syphilis Prevention and Control Plan (2010–2020) [
36] based on its national situation and relevant regulations, aiming to reduce the incidence of primary and secondary syphilis by 2020. However, the goal of controlling syphilis infection in China has yet to be achieved. Early prevention of syphilis can effectively stop its transmission. By identifying the spatial high-risk regions of syphilis incidence and its relationship with the socio-economic, health resource, and meteorological influencing factors in different regions may provide a deeper insight into early prevention and control strategies of syphilis. Based on the yearly incidence of syphilis during 2004–2017 in Ningxia, this study explored the spatiotemporal distribution of syphilis and investigated the association between the incidence of syphilis and meteorological factors, socio-economic, and health-resource. We found that the overall reported incidence of syphilis in Ningxia presented a yearly increasing trend, rising from 3.78/100,000 in 2004 to 54.69/100,000 in 2017, and this epidemiological trend was generally consistent with the findings of other regions in China [
14,
37,
38] and higher than the national incidence level (34.49/100,000) in 2017 [
7].
Spatial autocorrelation methods were used to analyze the spatiotemporal distribution characteristics of syphilis incidence in Ningxia from 2004 to 2017. There were clusters of syphilis incidence in Ningxia in 2007, 2009, 2010, 2011, 2012, and 2013. The “high–high” cluster areas were mainly in northern Ningxia (Helan, Jinfeng, and Pingluo), surrounding Yinchuan, the provincial capital of Ningxia. The “low–low” clusters were mainly located in southern Ningxia, with a tendency of distribution towards the central regions. This result was consistent with the findings of the spatiotemporal scan analysis, which confirmed that two spatial-temporal clusters were detected in Ningxia, the first cluster was identified during 2011–2017 in north of Ningxia (area radius of 149.84 km) and the second cluster was identified in south Ningxia during 2015–2017 (area radius of 35.63 km) with 2.94- and 2.57-times higher risk of syphilis than that found in other areas, respectively. The results of the three-dimensional trend surface analysis demonstrated that syphilis was more prevalent in the eastern and northern regions of Ningxia. It may be related to the continuous socio-economic development and change in people’s ideology in recent years; the gradual opening up of attitudes toward sexual behavior and presence of risky sexual behaviors results in a significant increase in the chance of infection contraction, which may explain the rapid increase in the number of syphilis cases [
14,
38]. Therefore, it is necessary to strengthen the early screening of syphilis in high-risk areas and conduct health promotion activities for high-risk population, which promote the use of condoms to minimize contact infection, establish correct sexual morality, and improve health awareness [
39,
40].
Regarding the factors influencing the spatiotemporal distribution of syphilis incidence, this study included meteorological, socio-economic, and health-resource indicators into the spatial error model for exploratory analysis. After adjusting for the effects of spatial autocorrelation, the results showed that the incidence of syphilis in Ningxia may be related to the tertiary industry GDP, per capita GDP, and the number of healthcare personnel. The incidence of syphilis in Ningxia may be positively correlated with the tertiary industry GDP and per capita GDP, while negatively correlated with the number of healthcare facilities and healthcare personnel. However, sex ratio and meteorological factors were not significantly associated with syphilis incidence in Ningxia.
Increasing 1 unit of tertiary industry GDP and GDP per capita may lead to an increase of 3.19 × 10
−7 and 4.38 × 10
−6 units of syphilis SMR, respectively. The socio-economic factors may play an important role in aggravating the high-risk spatial clustering of syphilis at the neighborhood level. With the rapid development of tertiary industry and the acceleration of urbanization, an increasing migrant population may be partially responsible for the high-risk regions located in the economically developed areas of north Ningxia. The research of related scholars [
41,
42] shows that, compared with other urban agglomerations in the northwest region, the inter-city flow in Ningxia along the Yellow City agglomeration is more obvious; the population mobility in the economically developed areas of Ningxia is increasing year by year, such as Yinchuan had a floating population of 418,500 at the end of 2018. In addition, Wu et al. [
43] found that the presence of migrant laborers was associated with primary/secondary syphilis infection in Shenzhen. Several empirical studies have also shown that subsets of rural-to-urban migrants have increased sexual risk [
21,
44,
45]. Thus, strengthening syphilis surveillance of migrant populations in the high-risk, economically developed, northern region of Ningxia may be an effective measure to effectively prevent syphilis. In addition, the spatial error model and spatial scan analysis also suggested that more prevention and control measures were needed to be disseminated to the neighborhoods of high-risk clusters.
Our results provided an insight into the relationship between allocation of health resources and incidence of syphilis in Ningxia. The incidence of syphilis was negatively correlated with the number of healthcare personnel. This may be related to the imbalance in the construction of medical institutions, recruitment of healthcare personnel, and the inadequate capacity for diagnosis and treatment of sexually transmitted diseases in medical institutions in each administrative area. It is suggested that rational allocation of medical resources can reduce the incidence of syphilis to a certain extent. Consistent with previous studies [
11,
39,
46,
47], developed areas may be able to provide high levels of coverage of health services and more effective approach to achieve syphilis health education, screening, and optimum treatment services. Therefore, the relevant departments should increase the allocation of health resources to the economically underdeveloped high-risk areas. Additionally, strengthening health education on syphilis and other sexually transmitted diseases, establishing health awareness among people, and promoting conscious adoption of healthy sexual behaviors may minimize viral infections caused by high-risk sexual behavior and may reduce the incidence of syphilis in Ningxia.
The current study has some limitations. First, this study did not provide a detailed sub-population analysis of the different stages of syphilis characteristics due to limited data; thus, we could not provide more precise recommendations for different sub-populations. Second, the data on influencing factors was limited by the data of covariates, such as education, urbanization rate, and population migration and it is recommended that more extensive and detailed research variables be selected for in-depth analysis in subsequent studies. Third, considering the serious health impact of syphilis on adults and its vertical transmission from mother to child, more attention should be paid to strengthening maternal surveillance efforts to minimize congenital syphilis; thus, further studies should address the spatial heterogeneity of congenital syphilis. Finally, this study was an ecological study examining the association between the incidence of syphilis and its influencing socio-economic and health-resource factors, the potential ecological fallacy is inevitable.