Sexually transmitted infections (STIs), which are also referred to as venereal diseases, have been public health threats for centuries due to their high morbidity and mortality in both high- and low-income countries. Economically, STIs impose a heavy burden on the health expenditure of both households and national health systems around the world. The physical and psychological consequences resulting from STIs are also associated with the worsening conditions of individuals’ well-being [1
]. Due to the malignant sexual, reproductive, and newborn health consequences, STIs impede sustainable human development in the 21st century.
As the biggest developing country in the world, China has been suffering from the epidemics of STIs for a long time. Among more than 30 STIs that can be infected or acquired predominantly through sexual contact, three are linked to the high incidence of illness and are therefore listed as the notifiable infectious diseases, which are highlighted in the Law of the People’s Republic of China on the Prevention and Treatment of Infectious Diseases
]. Of the three notifiable sexually transmitted infections, two are classical STIs and currently curable, namely syphilis and gonorrhea, and one is human immunodeficiency virus (HIV)/AIDS that is incurable but susceptible to mitigation through treatment [3
]. It is important to note that there are still other routes of transmission (blood, mother-to-child) of HIV/AIDS, but its transmission by sexual activities displays a substantial increase and has become a primary transmission mode in China recently [4
]. According to the China Health and Family Planning Statistical Yearbook 2016 [5
], syphilis, gonorrhea, and HIV/AIDS were all fairly active all over the country in 2015, with their reported cases ranking the third (433,974 reported cases), fifth (100,245 reported cases), and eighth (50,330 reported cases) among all of the 42 notifiable infectious diseases, respectively.
In literature, the academic world has been committed to improving policy designing for the control and prevention of notifiable STIs in China. First of all, the epidemiologic trends of STIs have always been the focus of numerous scholars. For instance, Chen et al. [6
] reviewed the epidemiologic trends of STIs in China based on the national system of STI surveillance and concluded that the epidemic pattern of STIs in China is different from that in developed countries. Li and his colleagues [7
] retrospectively studied the HIV/AIDS morbidity, mortality, and also the case fatality rate in China from 2004 to 2011. Tan et al. [8
] used wavelet transformation and Fourier analysis to assess the temporal trends of monthly reported syphilis and gonorrhea cases in Guangdong province. Yan et al. [9
] investigated the shift in the epidemiological features of HIV/AIDS in Fujian province. The epidemiologic trend analyses provided important evidence for understanding the epidemic situation. However, the temporal analysis alone is not enough for the making of targeted control programs.
In recent years, scholars have paid more and more attention to the spatial distribution of STIs epidemics in China. Peng et al. [10
] applied spatial autocorrelation analysis to study the spatial distribution of HIV/AIDS in the Yunnan province. Targeted at Shenzhen, Wu et al. [11
] conducted a spatial clustering analysis on the primary/secondary syphilis cases and detected the high-risk areas for spatially targeted control measures. Qian and his colleagues [12
] introduced 17 provincial variables to the hierarchical clustering analysis for forming HIV/AIDS sub-epidemic areas in China. Zhang [13
] analyzed the distribution patterns of the HIV/AIDS epidemic in a western provincial unit and explored its relationship with economic input factors. Chen et al. [14
] implemented Kulldorff’s spatial scan statistic to identify spatial clusters of risky sexual behaviors and STIs in Guangzhou. Additional spatial analysis can be found in certain population groups, such as the HIV/AIDS spatial analysis among the elder adults (≥50 years old) in China [15
], and spatial temporal analysis on the HIV/AIDS epidemic among young people (15–24 years old) [16
Despite the accumulation of knowledge, few studies did a comprehensive spatial-temporal analysis on all of the notifiable STIs or compare their spatial changing patterns. However, the comparison of different spatial changing patterns of all of the notifiable STIs is of great importance for their prevention and control. The reasons can be twofold: firstly, the correlations of different STIs should not be ignored, many studies have proven that STIs can expedite the disease processes of each other, and many STIs even facilitate the acquisition of HIV/AIDS [15
]. Secondly, unlike other infectious diseases, STIs share the same route of infection, similar high-risk population groups and overlapping prevention and control measures, which provides great possibilities for their combined prevention and treatment. This study is initiated to detect, describe, and compare the spatial-temporal clustering of notifiable STIs at the provincial level and to relate spatial analysis results (global and local) to epidemiologic trends during the past decade, we hope that this study can provide more region-oriented evidence for control and prevention policy making of STIs in China.
In order to improve the knowledge of notifiable STIs prevention and control in China, the investigation of epidemiologic trends and spatial changing patterns are of vital importance. Nevertheless, existing studies paid little attention to the comparison of different STIs’ spatial changing patterns and seldom related them to epidemiologic trends. The findings of this study, therefore, supplement previous studies and serve as references for policy makers to develop disease-combined and region-oriented STI control and prevention strategies.
First of all, we would like to compare the epidemiologic trends and overall agglomeration level of the three notifiable STIs. As for the former, this study further extends the study of Zhang and Wilson [27
], who reviewed the trends in notifiable infectious diseases before 2010 and discovered the different epidemiologic trends in notifiable STIs. As reported previously, the nationwide incidence rate of HIV/AIDS increased dramatically during 2005–2015, that of syphilis has also been growing but with a slower speed during the same time. In comparison, the incidence rate of gonorrhea dropped at first but remained stable in the second five years. However, the epidemiologic trends differ greatly between provincial units, thus resulting in the changes in agglomeration level and clustering areas. The results of global Moran’s I indicate that the incidence rate of all the notifiable STIs tended to aggregate at the provincial level. The significant global Moran’s I of gonorrhea, syphilis, and HIV/AIDS at most observation time points meet our expectations as the spatial cluster feature is an inherent attribute of the infectious diseases. It is also consistent with other studies on the STIs [15
]. However, the trends of global Moran’s I reflect the diverse spatial distribution characteristics of notifiable STIs. The rapid increase in the incidence of HIV/AIDS is accompanied by the swift growth of its global Moran’s I, indicating the ever increasing unevenness and deteriorating conditions in the geography of HIV/AIDS epidemics (certain regions are more plagued with the disease and it has been expanding to surrounding regions). In comparison, the agglomeration level of syphilis decreased during the whole period, with its global Moran’s I reducing from 0.3789 in 2005 to 0.1099 in 2015. It is worth mentioning that the global Moran’s I of gonorrhea showed a slow growth despite the decreasing trend of its incidence. To conclude, the rapid increase of HIV/AIDS and syphilis incidence, as well as the stable incidence of gonorrhea, revealed the serious situation of STIs prevention and control confronting the Chinese health sector. The reasons can be twofold. First, higher levels of population mobility in contemporary China have significantly multiplied the possibility of STI transmission. This does not only involve the labor migration, but also the mobility of female sex workers [28
]. Besides, the emergence of antimicrobial resistance in all bacterial STIs and the particular problem of resistant gonorrhea present a challenge to STIs prevention, control, and elimination [29
Secondly, the summary of the spatial cluster frequency provides important evidence for targeted prevention and control programs. The results of local spatial autocorrelation analysis, i.e., detection of spatial clusters, have confirmed the significant spatial variation in STIs epidemic at the provincial level and specified two priority areas: south-western border area (Yunnan, Guangxi) and the Yangtze River Delta region (Zhejiang, Shanghai, Jiangsu). It means that the clusters of STIs have gone beyond the provincial level and exhibited a trend of regionalization. Among the three STIs, HIV/AIDS is particularly prominent in the former region, while gonorrhea and syphilis in the latter. In 2015, Yunnan and Guangxi were the only two provincial units whose incidence rate of HIV/AIDS exceeded 10/100,000. It is in he Yunnan province that the first case of HIV/AIDS was discovered in 1985 in China [10
]. One of its underlying causes is probably the heroin trafficking route starting from the “Golden Triangle”, which opens the door for HIV/AIDS transmission in China. There are a large number of injection-drug users in Yunnan and the illegal trade across the borders is rampant. In addition, the high mobility of a mass population might be accredited as the catalyst for the high incidence of HIV as well. The border provinces are insufficient in prevention measures, and therefore quite a number of the population are exposed to high-risk behaviors, namely, incorrect use of condoms, etc. [30
In comparison, the Yangtze River Delta region is the clustering area of both gonorrhea and syphilis. It is one of the three most integrated and dynamic city-regions in China, consisting of four provincial units, i.e., Anhui, Jiangsu, Zhejiang, and Shanghai. In addition to Shanghai, the core city, there are a number of regional center cities, such as Hangzhou and Nanjing. Other cities such as Wenzhou, Ningbo, Wuxi, and Suzhou are also highly developed. In 2005, the HH clustering areas of syphilis mostly overlapped with that of gonorrhea, while their differences lie in the spatial-temporal changing patterns. The HH cluster areas of gonorrhea have been expanding while the other one has been shrinking. The incidence rate of gonorrhea in Shanghai, Jiangsu, and Zhejiang showed a HH cluster feature and were significant at every time point, with Fujian also being significant in 2015. In comparison, the HH cluster feature of syphilis in the three provincial units shrank, and finally disappeared completely.
Last but not least, there are some interactions between the epidemiologic analysis and the spatial-temporal analysis. In effect, the changes of agglomeration level and spatial-temporal clusters result from the unbalanced growth of the incidence of STIs. Therefore, we would like to discuss the results with a combination of the epidemiologic trends and spatial analysis. Generally, the epidemiologic trends and global Moran’s I make us better understand the STIs situation. When considered together, the growth rate of STIs incidence and the changes in Global Moran’s I imply relatively different scenarios for each STI. For instance, a decreasing incidence and an increasing global Moran’s I (gonorrhea) indicate the deteriorating situation in cluster areas; increasing incidence and decreasing global Moran’s I (syphilis) indicate the gradually spreading of the epidemic and an increase in incidence rate in most provincial units. Specifically, the spatial-temporal cluster analysis of incidence rates also provides implications for the phases of the STIs epidemics in some provincial units from a geographical perspective. For instance, owing to the high incidence and high growth rates in Yunnan, the incidence rate of HIV/AIDS in the Sichuan province, its neighboring province, increased 1664% during 2005–2010, the biggest jump among all of the provincial units. In like vein, during 2010–2015, the incidence of gonorrhea in most provincial units declined, while the continuously increasing incidence in Jiangxi (2%), Shandong (39%), and Henan (48%) can be attributed their geographical proximity.
To date, STIs have become one of the major challenges faced by the Chinese health sector. However, it is not the first time that the Chinese government faces the STI challenge. Before the founding of the People’s Republic of China, STIs were widespread, especially among the female sex workers in big cities [6
]. Since the early 1950s, the Chinese government attacked STIs with massive treatment campaigns and structural measures, such as (1) the establishment of specialized agencies, (2) strikes on commercial sex, (3) reeducation camps for sex workers, and (4) increasing the availability of the diagnostic and treatment services [31
]. Through 15-year efforts, STIs were officially reported eradicated in China by 1964. However, in the 1980s, STIs emerged again after China’s reform and opening-up policy [14
Fortunately, the rapid development in screening technology brings great convenience for STI surveillance. Owing to China’s family planning policy, testing after marriage has become regular, which enables the Center for Disease Control and Prevention to document the health conditions for married women. However, the testing for unmarried men and women is still insufficient. Without basic knowledge of STIs, many people are diagnosed STIs when they have serious symptoms. Since STIs are highly private and the cultural atmosphere in China is rather conservative, knowledge promotion of STIs is restricted to sex education in communities. Little publicity of STIs has been seen on social media and other new media. What is worse, rapid urbanization, the growing mobility of the population, and changes in sexual behaviors result in a great difficulty of STIs prevention and control. By far, the most important tool to assist the control of STIs is early diagnosis and treatment of those infected, and therefore current STI prevention and control measures mainly focus on MARPs, such as the drug users, female sex workers (FSWs), and Men who have sex with men (MSM) [11
]. Nevertheless, evidence from the epidemiologic trends and spatial changing patterns provide two new dimensions for targeted interventions, with its advantage lying in the detection of priority areas at a specific temporal-spatial spot for infectious diseases prevention and control. By means of the spatial-temporal data analysis, the government can not only focus on the MARPs, but also the most-at-risk areas (MARAs) and most-at-risk timings (MARTs). On the one hand, based on the spatial changing patterns of notifiable infectious diseases and the cluster frequency maps, southwest China, Yangtze River Delta region, some other border regions, and also their neighboring provincial units are the most-at-risk areas (MARAs), which should be the top priority areas for STIs prevention and control in China. In addition, the MARAs with more cluster frequency demand more attention and call for more disease-combined intervention programs. On the other hand, even though two geographical units may have similar incidence rates of STIs, they might be at totally different time points of the epidemiological trends, therefore the control and prevention measures should be tailored to the rising trend and epidemic season (MARTs) of epidemics.
With a limited scope and data availability, this study only targets STIs at the provincial level in China. However, the epidemiologic trends and spatial changing patterns of STIs are often across scales. Zooming into smaller scales, researchers may find more delicate distribution and clustering patterns of STIs, and therefore come up with more specific and solution-specific findings. Besides, the control and prevention of STIs require concerted efforts across scales. Covariates are also important for the analysis of the epidemiology of STIs, which is not the focus on this study. Hence, we call for future inter-scalar research on the distribution patterns and epidemiology trends of STIs.
China’s national health would be in jeopardy without effective control of infectious diseases. However, the prevention and control of each kind of infectious diseases on such a large territory is never an easy task. In this retrospective study, the notifiable STIs exhibit various temporal-spatial distribution characteristics among the provinces of China. Syphilis and HIV/AIDS, especially the latter, displayed a strong upwards trend, indicating that it is time to tackle with STIs more seriously.
To address the outbreaks of STIs, collaboration across provincial boundaries should be initiated through effective institutional arrangements, such as collaborative policy design for regional-oriented prevention and control measures. First, we propose the regional preference for the prevention and control programs. For instance, free condom distribution should increase in these priority areas and epidemic seasons, sex/health education should be enhanced, particularly at targeted regions, and most at risk populations (for instance, college students and migrants). Second, the STIs prevention measures should not be limited to the existing programs. For instance, rational sex education course in compulsory education should be guaranteed and optimized. Besides, promotion on television, mobile phones, and the Internet should be mobilized to spread the knowledge on STIs prevention and control.