Toward tuberculosis elimination by understanding epidemiologic characteristics and risk factors in Hainan Province, China

Through understanding the epidemiological characteristics and risk factors of TB last decade in Hainan Province, this study enhanced the knowledge on current epidemic of TB in Hainan Province to provide scientific suggestions and references for local TB elimination work.

TB notification rate varied with the time and space correlated with migrant and minority population

The epidemiological study analyzed the spatial–temporal distribution of TB in Hainan Province from 2013 to 2022, and showed following four feature. Firstly, with the implementation of the TB control programme since 2014, the TB notification rate in Hainan Province has decreased significantly and maintained a stable downward trend. The supported by the fact that a total of 64,042 TB cases were notified in Hainan Province from 2013 to 2022, the number of TB cases and pathogen-positive cases notified in 2022 decreased by 37.52% and 19.63% compared with that in 2013, respectively. However, the average annual notification rate of TB in Hainan Province was 62.36/100,000, which was higher than the national average level, so that more harder efforts are necessary to mitigate the relatively high risk of TB facing in Hainan Province [9]. This decline trend of TB transmission could potentially be attributed to the adoption of the "integrated" TB control framework in China, wherein specialized TB hospitals assumed the roles of diagnosing, treating, and overseeing TB cases. This integrated approach has markedly enhanced the efficiency of TB prevention and management, and TB control programme in China and Hainan has gradually improved [6, 25].

Secondly, the TB notification rate was higher in some regions of Hainan Province, particularly among males, old people, and farmers. The prevalence of TB in Hainan Province showed no significant seasonality presented in the spatial–temporal distribution study. However, the TB notification rate was relatively higher during spring, possibly due to the climate change and environmental variation [7, 8]. The central and southern regions of Hainan Province exhibited higher TB notification rates, which are largely attributed to their higher population density, weak economic conditions, and limited access to medical resources [26, 27]. The results of study by Christian et al. and Knut et al. showed that people contact can increase the spread of TB, and people with low socioeconomic level were more likely to develop TB due to poor living conditions and weak health awareness [26, 27]. The notification rate was higher in people over 60 years old, and the males with a higher proportion surpassed the global and Chinese averages, which likely linked to local male lifestyles, working environments, and personal health management. Particularly unique habits, like more social gatherings, among the males in Hainan Province may increase their susceptibility to TB infection. Additionally, unhealthy habits such as smoking and alcohol addiction can weaken male immunity, elevating the risk of TB [10, 28]. Li et al. also found that men in Hainan Province had the custom of gathering to drink tea and chat, which aggravated the spread of TB [10]. Moreover, the males may show lower health awareness and engage in fewer regular check-ups [29]. The proportion of farmers among TB patients was also relatively high, possibly due to the poor living conditions in rural areas [26].

Thirdly, the unique characteristics of migrate population frequently traveling to Hainan Province have become the bridge for spreading TB transmission. It supported by fact that imported cases mainly originated from Sichuan Province, Heilongjiang Province, Hunan Province, Guangdong Province, and Guangxi Zhuang Autonomous Region, which was in consistence with the provinces where majority of migrant came from [30] as well as the high TB notification rate observed in these regions [16, 23]. The number of migrant cases was relatively low in January and February, possibly due to the Chinese New Year, during which many migrant workers may return home to reunite with their families [9]. The study by He et al. showed an association between cross-domain population migration and TB incidence [16]. Firstly, population migration increases the contact between people, and the risk of infectious diseases such as TB increases greatly. Secondly, population migration in China is often from areas with a low level of economic development to the high, and people in areas with a low level of economic development are more likely to carry Mycobacterium tuberculosis [16, 31]. TB primarily spread through airborne transmission, and the interprovincial mobility of these cases could potentially facilitate TB transmission between regions, posing a hidden risk of TB outbreaks in Hainan Province [16, 31].

Fourthly, TB patients in Hainan Province were mainly found passively, with low positive detection rate and delay in seeking medical care. It is noticed that bacteriologically negative patients were more than positive patients, which still possess a certain degree of infectivity and may have a certain impact on TB prevalence in the community [32]. The median duration of patient delay in seeking medical attention for TB patients in Hainan Province was 30 (10, 61) days, higher than the national average [33]. Among different occupational groups, students had lower duration of patient delay, likely because they have easier access to relevant health education and medical resources, enabling them to seek diagnosis and treatment earlier [34]. Additionally, the delay in seeking medical attention was lower among the Han ethnic group compared to minority ethnic groups like the Li people, possibly due to cultural differences between different ethnic groups, unequal distribution of medical resources, and varying levels of awareness of TB [35, 36].

Correlation between TB notification rate and socio-economic status

The investigation employed with GTWR model showed that the impact factors of TB notification rate in Hainan Province were more likely associated with social and economic indicators. Results showed that per capita GDP (factors reflecting the economic development level) and number of medical institutions and health personnel per 10,000 population (factors reflecting the level of medical and health services) mainly influenced the high TB notification rate in some cities and counties of Hainan Province. Additionally, other risk factors may also exist in some cities and counties. For example, Qiongzhong County and Wanning County should pay attention to the TB prevention and control situation among their rural populations.

Firstly, lower per capita GDP in most areas was associated with higher TB notification rates. TB prevalence is not only a medical issue but also a social issue. Economically developed regions have higher population densities but better natural conditions, more advanced medical facilities, and higher levels of TB prevention and control knowledge, resulting in lower TB notification rates. Conversely, economically undeveloped regions have a lower population density but relatively abundant per capita medical resources. However, the uneven development of regional economy contributes to spatial differences in TB incidence in the study area [37,38,39], due to limitations imposed by the natural environment, educational level, and customs, TB prevention and control efforts may not yield immediate results in these regions [26]. Previous studies have revealed associations between TB and per capita GDP, poverty, living standards, and malnutrition [26, 27]. Christian et al. and Knut et al. suggested that most risk factors for TB were associated with social conditions. People from lower socioeconomic groups generally have more contact with people with active disease, are more likely to live and work in crowded environments, have lower levels of health awareness, and have less access to quality health care than people from higher socioeconomic groups [26, 27]. A European study showed that disparities in TB prevalence were due to uneven economic development. There was a significant negative correlation between GDP and TB incidence [40, 41].

Secondly, the higher the number of medical institutions and health personnel in the central and some developed cities of Hainan Province, the lower the TB notification rate. The number of medical and health institutions and health personnel can reflect the level of medical security and the treatment capacity of the medical system to some extent. The greater the number of medical and health institutions and health personnel, the higher the level of health services can be used to detect TB earlier and reduce its transmission [6, 40, 42]. Both studies by Zhang and Wang et al. showed a close relationship between the level of medical resources and TB notification rate. Insufficient medical resources can not screen more potential TB patients, and the prevention and control of TB patients is also weak, resulting in the transmission of TB can not be effectively interrupted [40, 42]. The results of GTWR provided a possible scientific reference for regional TB prevention and control efforts, contributing to the improvement and achieving the goal of precise prevention and control measures.

Projection patterns for TB elimination in Hainan Province

This study also predicted the future prevalence of TB in Hainan Province, and the results showed that the 2035 (Rate < 10/100,000) and 2050 (Rate < 1/100,000) targets set by WHO would not be reached if the current intervention strategy is not changed with the same downward trend of TB notification rate. Therefore, the prevention and control of TB in Hainan Province needs to be further strengthened in the future, insisting on highlighting key points, adapting measures to local conditions and guiding according to classification. The Chinese government has further issued the Guiding Tuberculosis Control Through the Healthy China Initiative 2019–2030 to guide local prevention and control work [43].

Based on the above research results, first of all, the following strengthening measures for TB elimination in whole Hainan Province were proposed: (1) TB screening in key populations, (2) prevention and control of TB in migrant population, (3) active surveillance. Firstly, it is recommended that local TB screening be strengthened in key populations, expand screening coverage for key groups such as males, people over 60 years old, and rural populations. Secondly, it is necessary to promote the prevention and control of TB in migrant population, strengthen inter-departmental cooperation, improve the working and living conditions of migrant population in densely packed places, strengthen environmental health improvement, and carry out symptom screening. Thirdly, active surveillance should be strengthened, and the designated TB medical institutions, disease control institutions and primary medical and health institutions should strengthen cooperation, and timely TB examination should be carried out for the symptomatic patients. The application of new diagnostic techniques is promoted to improve the positive detection rate of pathogens in TB patients.

Secondly, the annual decline rates of high, medium and low groups would be 15%, 12% and 11.5%, respectively, before 2035 to achieve TB elimination targets. It is necessary to further analyze the characteristics of local epidemic and carry out tailored and precise prevention to reduce the risk of TB in Hainan Province. (1) Regions with low TB notification rate need more TB specialized hospitals to provide more adequate medical services, and more attention should be paid to the TB epidemic of migrant population outside the province and in other cities in the province. Since the establishment of free trade port in Hainan Province, cross-border population migration has increased. It is necessary to establish and improve the epidemic information reporting system. Health education activities on TB prevention and control were held regularly in the gathering places of migrant population, and environmental sanitation was improved. (2) The regions with medium TB notification rate, like Qionghai City and others, need to improve the level of medical and health services, increase TB specialized hospitals and health personnel. (3) In regions with high TB notification rate, more attention should be paid to TB prevention and control in rural and poor population, and more TB specialized hospitals and health personnel should be provided to improve the level of medical services. Comprehensive universal TB census and centralized isolation and treatment of patients with infectious disease should be carried out to promote the rapid decline of TB cases. Focusing on TB prevention and control in these regions will help Hainan Province achieve TB elimination.

In addition, combined with the Global Plan to End TB (2023–2030) [44], Hainan can also strengthen TB screening in students, diabetes patients, people living with HIV/AIDS. To curb the further development of drug-resistant TB, improve the laboratory diagnostic capacity of drug-resistant TB, and promote the standardized diagnosis and treatment of drug-resistant TB. Scientific research on TB should be intensified, new vaccines should be developed, and the protective efficacy of vaccines should be improved.

Furthermore, the COVID-19 pandemic had a continued negative impact on the accessibility of TB diagnosis and treatment services from 2020 to 2022, as well as the burden of TB [1, 2]. The results of this study indicated a considerable reduction in the TB notification rate starting from 2020. This decline could be attributed to an increased number of undiagnosed and untreated TB patients as a consequence of the pandemic's impact. With the outbreak of COVID-19, diagnostic services were disrupted due to TB staff supporting the prevention and control of the COVID-19 epidemic, resulting in insufficient TB services and an overloaded healthcare system. Consequently, laboratories might have struggled to diagnose TB and other diseases in a timely manner. Moreover, COVID-19 related isolation and lockdown measures have made it more difficult for TB patients to seek medical attention promptly, leading to delays in diagnosis and treatment [45, 46].

This study had certain limitations. Firstly, Hainan Province is a tourist attraction in China with high population mobility, which increases the difficulty of TB prevention. The study only obtained rudimentary information about migrant population without details on residence time and the size of migrant population, which may result in relatively biased analyses of related factors. Secondly, TB may also be influenced by individual lifestyle habits, regional customs, and other potential factors. These factors were not comprehensively controlled in this study, potentially leading to biased results. Third, there was a lack of field studies on specific populations to obtain the evaluation of the effect of the current measures. To gain a more comprehensive understanding of TB transmission and prevention, future research may consider further analysis of the impact of migrant populations on TB transmission and corresponding field studies to understand their individual living habits, regional customs, and existing TB prevention, evaluate current measures, and improve TB control through interventions.

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