1. Introduction
Tuberculosis (TB) is the ninth leading cause of death worldwide and the leading cause of death from a single infectious agent, ranking above HIV/AIDS [
1,
2]. According to the 2017 Global Tuberculosis Report, 10.4 million people fell ill with TB in 2016, and 1.7 million people died from the disease (including 0.4 million people with HIV) [
2]. China is one of 22 countries with the heaviest burdens of TB patients, with the third highest number of cases [
2]. However, highly complex dynamics and spatial heterogeneity are associated with TB in China at the provincial level [
3,
4,
5,
6]. Zhejiang, as a province located in eastern China, is a highly socioeconomically developed province [
7]. The province has 11 prefectures: HZ (Hangzhou), QZ (Quzhou), HUZ (Huzhou), JX (Jiaxing), SX (Shaoxing), ZS (Zhoushan), LS (Lishui), WZ (Wenzhou), TZ (Taizhou), JH (Jinhua), and NB (Ningbo). In recent decades, the TB incidence rate of Zhejiang province has decreased slowly from 2008 (71.50/100,000) to 2017 (47.54/100,000) and has remained at a modest level in China [
7]. However, there are still 27,000 TB cases in Zhejiang every year due to the large population (55 million) [
8].
According to a large number of school TB outbreak reports, clustering epidemics commonly occur, especially in senior schools and universities [
9]. In China, students with TB accounted for 4.02% of total TB patients in 2014 [
10], and TB outbreaks often occurred. Teachers who work in schools are at risk of being infected with TB or to becoming a source of infection [
11]. For example, consider an outbreak that occurred in California. A teacher who developed multidrug-resistant TB (MDR-TB) was exposed to dozens of children, infecting 31 children with TB [
12]. Therefore, it is important to monitor TB epidemics among full-time teachers. According to a study carried out in one prefecture of Zhejiang province, the average annual reported incidence rate of active TB among full-time teachers (39.15/100,000) was higher than that of active TB among students (22.34/100,000) from 2005 to 2011 [
13]. Another study in one county of Zhejiang province also demonstrated that the average annual reported incidence rate of active TB among full-time teachers (25.42/100,000) was about 2.5 times higher than that of active TB among students (10.56/100,000) from 2005 to 2012 [
14]. However, the TB incidence rate among full-time teachers in whole province has not been studied in China, and the baseline data is very limited.
Based on the “National Tuberculosis Information Management System” (NTIMS) (established in 2005), we conducted this retrospective study among full-time teachers to (1) understand the baseline TB incidence rate among full-time teachers in Zhejiang province, (2) explore the epidemiological distribution and clinical characteristics of full-time teachers with TB and (3) provide evidence on TB prevention and control practices among full-time teachers in schools.
2. Data Collection
The NTIMS, which was established in 2005, provides a chance for us to analyze TB epidemics among full-time teachers in Zhejiang province (
Figure 1) in the past 10 years. NTMIS records the demographic information, disease features, case-finding pattern and treatment outcome of each patient. We collected demographic and disease data for each teacher case with TB, including gender, age, nationality, habitation, sputum smear test results, time of TB symptom onset, time of diagnose, treatment classification, diagnose result, case-finding pattern, strategy of patient management and treatment outcome. The data we extracted covered the period from 1 January 2005 to 31 December 2016. We collected the annual population data for full-time teachers in 11 prefectures from the Education Yearbook of Zhejiang Province, which recorded the statistics for educational development, general administration of education, educational personnel management, basic and higher education and education examinations etc. [
15]. Due to a lack of population data on the age and gender of full-time teachers in the Education Yearbook of Zhejiang Province, we are limited to conduct further analysis of TB incidence rates of different ages, genders or other demographic characteristics among full-time teachers. The annual population data for Zhejiang province were extracted from the Statistical Yearbook of Zhejiang Province, which recorded the population, finance, employment, education, and environment and resources, etc. [
16].
2.1. Definitions
Case-finding delay: The time interval between the onset of TB symptoms and the first diagnosis of TB over 30 days [
17].
Health service-seeking interval: The time interval between the onset of TB symptoms and the first to visit the health provider [
18].
Diagnostic interval: The time interval between the first to visit the health provider and the first diagnosis of TB [
18].
Case-finding pattern: In our study, the case-finding pattern mainly includes direct visits to the designated TB hospital, referrals and tracking and physical examinations.
Direct visit to a designated TB hospital: Patients directly visit the designated hospital for TB when they have symptoms.
Referrals and tracking: Referrals mean that patients who directly visited a non-designated hospital for TB were referred to a designated TB hospital; tracking refers to health workers tracking TB cases to designated TB hospitals who have not been referred to designated TB hospitals.
Physical examination: Here the physical examination means that teachers screened chest fluoroscopy for TB and recommended to designated TB hospitals if they are suspected as TB cases.
Treatment classification: Including initial treatment and retreatment. The initial treatment refers to patients treated for TB for the first time; retreatment refers to the patients who were cured from TB and diagnosed again for TB.
Habitation: Including local and not local. In our study, local means patients whose permanent residence registered in Zhejiang province; conversely, not local means patients whose permanent residence is registered out of Zhejiang province.
Onset time of symptoms: The time when patients felt the symptoms of TB.
Adverse outcomes included treatment failure, transfer to MDR-TB treatment, death, treatment interruption due to side effects, and loss to follow-up.
2.2. Statistical Analysis
The incidence rates of both TB and pulmonary TB (PTB) among full-time teachers, students and the total population were calculated based on the total population, the full-time teacher population and the population of students in schools. The PTB incidence rate of the three groups was also calculated in 11 prefectures and is shown in a disease map. Chi-square analysis was used to analyze the relationships between epidemiological characteristics and clinical characteristics, case-finding delay, and treatment outcomes.
Descriptive analysis and univariate analysis were performed by Statistical Package for Social Sciences (SPSS) version 18.0 (SPSS Inc., Chicago, Il, USA). The inspection level of the Chi-test is 0.05. Line graphs and columnar diagrams were generated by Microsoft Excel. The map of incidence rates was generated with ArcGIS (version 10.3, ESRI, Inc., Redlands, CA, USA).
2.3. Ethic Statement
Ethics approval of this study has been obtained from the Ethics Committee of Zhejiang Provincial Centers for Disease Control and Prevention (2014–2017). We declared that we have kept all the private information confidential.
4. Discussion
By applying data from the NTIMS, our study is the first to present the epidemiological and clinical characteristics of TB among full-time teachers in China. We found that the incidence rate of TB among full-time teachers decreased during recent decades in Zhejiang province. According to the World TB Report 2017, the number of TB cases and the incidence rate of TB decreased gradually in China [
2]. The TB situation in Zhejiang province, among both the total population and full-time teachers, is consistent with this trend [
8], which indicates that TB prevention and control have achieved some progress in recent years [
8,
19]. The average PTB incidence rate was approximately 2.67 times lower than that of the total population. Compared to teachers, there are some other occupational groups such as farmers and migration workers with poor socioeconomic status having a higher TB incidence rate. On the other hand, there are few people over 65 years old among teachers and students while age over 65 was a risk factors of the TB incidence [
20]. Although teachers had a lower risk of TB than the total population, the average PTB incidence rate among full-time teachers from 2005 to 2016 was approximately 1.65 times higher than that of students, which indicated that teachers were at higher risk of TB than students in schools.
The results showed the geographical distribution of TB among full-time teachers in 11 regions of Zhejiang. The distribution pattern (high in the west and low in the east) was basically consistent with the distribution of TB among the total population in the province and the country [
7,
21]. Western Zhejiang, which mainly includes QZ and HZ, was a hotspot for TB among teachers. Accordingly, QZ has one of the highest disease burdens of TB in Zhejiang province [
21]. This high incidence may be related to the large proportion of agricultural populations and the relatively low economic development in QZ compared with those in other parts of Zhejiang [
22]. Hangzhou, as the capital city of Zhejiang, which has more migration workers from the western part of China, has a high incidence rate of TB among full-time teachers. In contrast, eastern Zhejiang, such as ZS, NB, and JX, which are located in the eastern coastal areas of Zhejiang province, have a high level of economic development [
22] and a low incidence rate of TB among both the total population and full-time teachers.
The results showed that the M:F ratio among full-time teachers with TB was 0.95:1, which is consistent with the results of Jun Li et al. [
13]. This ratio is very different from the M:F ratio among the total population [
20,
23,
24]. These results could be explained by the fact that female teachers account for the majority of the teacher population. Regarding age distribution, our study found that young and middle-aged teachers accounted for the majority of cases. The distribution is similar to that of TB among the total population [
25].
In general, direct visits to a designated TB hospital were the major case-finding mode for teachers with TB, followed by referrals or tracking. Only 3.00% of cases were detected by physical examinations. In fact, chest fluoroscopy for TB is a mandatory part of the physical examination for teachers in China [
26]. According to relevant rules, teachers in China will be suspended from work if they have TB [
26]. Therefore, teachers who are suspected to have TB may conceal their results and prolong the visiting period. Because early detection of TB is emphasized in the World Health Organization (WHO) End-TB strategy and teachers with TB could be an infection source for students in schools [
27,
28], we suggest that both schools and Centers for Disease Control (CDC) should take more measures to monitor and report full-time teachers with TB.
The case-finding interval was influenced by many factors, which mainly involved patients and medical institutions [
29,
30]. Our results show that 35% of full-time teachers with TB had a case-finding delay, and the mean case-finding interval was 45.3 days. The mean health service-seeking interval was 37.4 days, and the mean diagnostic interval was 11.4 days. Patients who are not diagnosed in a timely manner will be contagious for a long period of time, which will greatly increase the risk of group transmission [
31]. According to previous studies, the case-finding delay among full-time teachers with TB is shorter than that among typical PTB patients [
25,
32,
33], and the mean diagnosis interval was also shorter than those of PTB patients in Taiwan [
34], tuberculous meningitis patients [
35], and active TB patients after kidney transplantation [
36]. The case-finding interval among full-time teachers with TB was longer than that among PTB patients in Zhejiang province [
37]. In fact, both the case-finding interval and the health service-seeking interval among full-time teachers with TB were over 1 month, which accounts for most of the total delay. This phenomenon indicates that awareness about seeking health care needs to be improved among full-time teachers with TB. Moreover, our study showed that the proportion of case-finding delays increased with age. On the one hand, older teachers are more susceptible to chronic bronchitis, pneumonia and other diseases [
38]. Because the symptoms of PTB are difficult to distinguish from these diseases, TB is difficult to diagnose. On the other hand, poor knowledge about TB leads to delayed care-seeking [
18]. Young people may receive more TB health education in the new era of the internet. Such patients have more access to health services by using new technologies, such as mobile phone appointment systems. Our study also found that retreatment cases have a significantly higher proportion of case-finding delays than initial treatment cases. The initial treatment failure or side effects of drugs could lead retreated patients to lose confidence in treatment and cause a delay in seeking health care [
39,
40]. Regarding case-finding patterns, we found that patients detected by referrals or tracking and clinical consultations were prone to being delayed. Compared with physical examinations, referrals involve a more complicated process, which involves information transfer, personnel coordination and other factors, increasing the risk of a case-finding delay. The results of our study suggest that physical examinations could be an effective way to reduce this delay. It is also necessary to provide more health education and psychological counseling for retreatment patients to decrease delays.
The cure rate of full-time teachers with TB in our study was 77.10%, which is lower than that reported among all TB cases in China [
41] and in other countries [
42,
43]. The results showed that the cure rate of patients under full-course supervision is significantly higher than that of patients under self-administration. As members of an aggregated group, teachers need better treatment to recover early. Due to poor self-administration, it is necessary to strengthen the supervision and treatment of teachers with TB. Moreover, patients with different TB disease categories also differed in terms of cure rate. The cure rate of extra-pulmonary TB cases was lower than that of PTB and tuberculous pleurisy cases. Similar to PTB patients among the total population, retreatment TB cases among full-time teachers had a lower cure rate than initial treatment TB cases [
44]. Retreatment cases are at high risk of diagnostic delay [
45], and approximately 24% of cases will be transferred to MDR-TB [
46], thus contributing to the decreasing cure rate. With increasing age, the cure rate of full-time teachers with TB decreased. Aged patients are more prone to poor medication adherence and treatment adherence [
47]. In addition, some aged patients cannot seek health care in a timely manner due to limited mobility. These results indicate that we should pay more attention to the treatment and follow-up of older teachers with TB and retreatment patients with TB.
