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  • Open Access

Tuberculosis among migrant workers in Taiwan

Globalization and Health201915:18

https://doi.org/10.1186/s12992-019-0461-2

  • Received: 2 October 2018
  • Accepted: 20 February 2019
  • Published:

Abstract

Background

Although the worldwide incidence of tuberculosis (TB) has been slowly decreasing, the migrant workers remains an important gap for regional TB control. In Taiwan, the numbers of the migrant workers from countries with high TB incidence increase significantly in past decades and the impact on public health remains unknown. This study aimed to explore the difference of TB incidence between Taiwanese and the migrant workers.

Methods

The migrant workers are obligated to receive pre-arrival, post-arrival and regular chest X-ray screening during their stay in Taiwan. We retrospectively collected these data extracted from the Alien Workers Health Database in Centers for Disease Control, Taiwan from Jan. 1, 2004 to Dec. 31, 2013. Poisson regression models were used to compare the hazard ratios of TB between Taiwanese and the migrant workers after adjusting gender and age groups.

Results

The total migrant workers in Taiwan reached 314,034 persons in 2004 and 489,134 persons in 2013, accounting for 2% of Taiwan population. The TB incidence of migrant workers was similar to Taiwanese (53–73.7 per 105 vs 45.5–76.8 per 105). Comparing with Taiwanese, the TB risk was significantly lower in male migrant workers (HR: 0.76; 95% CI: 0.70–0.83, P < 0.001), but higher in female migrant workers (HR: 1.40; 95% CI: 1.35–1.46, P < 0.001). Besides, we found that the TB risk in migrant workers was 5.30-fold (95% CI: 4.83–5.83, P < 0.001) in youngest group (≤24 year-old) comparing with Taiwanese.

Conclusions

Migrant workers in Taiwan have higher TB incidence than Taiwanese in young groups, especially in females. The mainstay young laborers with latent tuberculosis infection risk is an important vulnerability for public health. Further investigation and health screening are warranted.

Keywords

  • Tuberculosis
  • Migrant workers
  • Latent tuberculosis infection
  • Foreigner workers

Background

Tuberculosis (TB) is the ninth leading cause of death worldwide, with most of them could be prevented with early diagnosis and appropriate treatment [1]. In 2016, there were 6.3 million new cases of TB globally [1]. Among the new cases, the top two incidence countries were India and Indonesia and the most TB-resistant countries were India and China [1]. Similarly, TB is one of the top infectious diseases and an important public health concern in Taiwan. The Bureau of National Health Insurance (NHI) in Taiwan introduced the no-notification-no-reimbursement policy to enhance TB notification and to decrease the incidence of TB since 1997 [2]. Accordingly, the NHI, which enrolled up to 99% of Taiwanese, has reached the TB notification rate more than 97% since 2007 [3, 4]. Also, the TB numbers (incidence) in Taiwan dropped from more than 16,000 cases (72 cases per 105 persons) in 2005 to less than 10,000 cases (41 cases per 105 persons) in 2017 [5].

Previous studies have shown that migrant workers from countries with a high incidence of TB have a significant impact on the epidemic of TB in low-incidence countries [68]. Pre-entry screening programs for tuberculosis in migrant workers is believed to be a high yield policy for active TB [9], though the risk of latent TB reactivation is persistent [10, 11]. The average annual TB notification rate is reported to be higher in the foreign-born population than the Taiwan-born population [12]. In addition, the numbers of the migrant workers in Taiwan from countries with high TB incidence increase significantly in past decades [5]. Although the migrant workers have to receive pre-entry screening and post-arrival regular health check-up, to date, little is known about the TB incidence and the characteristics of TB population of the migrant workers in Taiwan. Therefore, this study aimed to explore the difference of TB incidence between Taiwanese and migrant workers. Also, the study aimed to compare the gender and age differences of TB burden in Taiwanese with the migrant workers.

Methods

Design

The profile of the general population of Taiwanese was obtained from the official publications of the Ministry of the Interior, Taiwan [13]. The incidence rate of TB detected in each origin countries were estimated by the WHO [14]. The profile of migrant workers was extracted from the National Immigration Agency where the number of persons entering and leaving Taiwan were recorded and stratified by country of origin, gender and age [15]. Since TB is a notifiable disease by the Law on the Control of Communicable Diseases in Taiwan, data of all TB cases in Taiwanese notified between January 1, 2004 and December 31, 2013 were obtained from the National TB Registry [16]. All migrant workers were obligated to receive pre-arrival, post-arrival (within 3 days after arrival) and regular chest X-ray screening (6th, 18th and 30th month after arrival) during their stay in Taiwan [17]. Besides, all migrant workers were seronegative of human immunodeficiency virus (HIV) before their entry and were excluded from the study once diagnosis of HIV infection. Also, we retrospectively collected TB cases from Alien Workers Health Database in Centers for Disease Control, Taiwan [18]. The epidemiological records in their native-born countries were extracted from annual reports in World Health Organization [19]. The design of the study was approved by the Research Ethics Committee in National Taiwan University Hospital (201807018W) before the study was conducted.

Case definition

TB in Taiwan was diagnosed by two approaches: 1) laboratory diagnosis: human specimens which was smear-positive for acid-fast bacilli and/or culture-positive for Mycobacterium tuberculosis including sputum, body fluid and tissue; 2) clinical diagnosis by specialists: the clinical and radiographic manifestations were compatible with TB, the patient was received detailed evaluation to exclude other diagnoses, and the patient has initiated treatment with more than one anti-tuberculosis drugs [19].

Statistical analysis

The baseline categorical data were presented by frequency with percentages. The TB incidence was defined as the number of events divided by the follow-up person-years, which were calculated as the time from 2004 to the diagnosis of TB, death or the end of 2013. We used Poisson regression models to assess hazard ratios (HRs) and 95% confidence intervals (CIs) of TB for the Taiwanese compared to the migrant workers after adjusting gender and age groups respectively. All 2-sided p values were presented. All analyses were computed using the SAS version 9.4 (SAS Institute Inc. Cary, North Carolina).

Results

The total migrant workers in Taiwan reached 314,034 persons in 2004 and 489,134 persons in 2013, accounted for 2% of Taiwan population. The mainly import countries were Indonesia, Philippines, Thailand, and Vietnam in Fig. 1. From 2004 through 2013, 2256 new cases of TB were found among migrant workers during their regular health examination in Tables 1 and 2. The TB incidence of the migrant workers was similar to Taiwanese. (53–73.7 per 105 vs 45.5–76.8 per 105) From 2004 to 2013, the annual TB incidence in Taiwanese has been decreasing whereas the annual TB incidence in migrant workers has been increasing in Fig. 2. Therefore, the TB incidence of migrant workers exceeded Taiwanese since 2012.
Fig. 1
Fig. 1

Annual numbers of the migrant workers in Taiwan, 2004–2013

Table 1

The incidence of tuberculosis among Taiwanese and the foreign laborers during 2004–2013

 

Taiwan

All foreign laborers

Case

Population

Incidencea

Case

Population

Incidence

2004

16716

22689122

73.7

143

314034

45.5

2005

16472

22770383

72.5

168

327396

51.3

2006

15378

22876527

67.4

188

338755

55.5

2007

14480

22958360

63.2

190

357937

53.1

2008

14265

22037031

62

239

365060

65.5

2009

13336

23119772

57.8

193

351016

55.0

2010

13237

23162123

57.2

196

379653

51.6

2011

12634

23224912

54.5

257

425660

60.4

2012

12338

23315822

53

342

445579

76.8

2013

11528

23375517

49.4

340

489133

69.5

Averageb

379422

aPresented with annual incidence with cases/ 105

bThe annual average numbers of the immigrant workers

Table 2

The incidence of tuberculosis among Taiwanese and the foreign laborers by different countries during 2004–2013, stratified by countries

 

Indonesia laborers

Philippines laborers

Thailand laborers

Vietnam laborers

Case

Population

Incidencea

Case

Population

Incidence

Case

Population

Incidence

Case

Population

Incidence

2004

26

27281

95.3

41

91150

45.0

48

105281

45.6

28

90241

31.0

2005

19

49094

38.7

75

95703

78.4

51

98322

51.9

23

84185

27.3

2006

31

85223

36.4

72

90054

80.0

54

92894

58.1

31

70536

43.9

2007

56

115490

48.5

61

86423

70.6

41

86948

47.2

32

69043

46.3

2008

74

127764

57.9

68

80636

84.3

62

75584

82.0

35

81060

43.2

2009

77

139404

55.2

48

72077

66.6

34

61432

55.3

34

78093

43.5

2010

77

156332

49.3

56

77538

72.2

33

65742

50.2

30

80030

37.5

2011

111

175409

63.3

80

82841

96.6

37

71763

51.6

29

95643

30.3

2012

163

191127

85.3

75

86786

86.4

55

67611

81.3

49

100050

49.0

2013

152

213234

71.3

75

89024

84.2

55

61709

89.1

57

125162

45.5

Averageb

128036

85223

78729

87404

aPresented with annual incidence with cases/ 105

bThe annual average numbers of the immigrant workers

Fig. 2
Fig. 2

Tuberculosis incidence (persons per 105) among the migrant workers, their native countries and Taiwan

Comparison of TB incidence among migrant workers and Taiwanese by different countries and genders are shown in Table 3. Comparing with Taiwanese by different countries, the TB risk was significantly higher in Philippines (HR: 1.22; 95%CI: 1.15–1.30, P < 0.001) but lower in Vietnamese (HR: 0.57; 95%CI: 0.47–68, P < 0.001). Comparing with Taiwanese by different genders, the TB risk was significantly lower in male migrant workers (HR: 0.76; 95% CI: 0.70–0.83, P < 0.001), but higher in female migrant workers (HR: 1.40; 95% CI: 1.35–1.46, P < 0.001).
Table 3

Comparison of TB incidence among foreign laborers and Taiwanese, stratified by gender, 2004 to 2013

 

Tuberculosis cases

Average incidencea

Hazard ratio

P value

All

 Taiwan

140384

61.1

1.00

 

 All migrant workers

2255

58.4

0.97(0.93–1.01)

0.1846

  Indonesia

786

60.1

1.00 (0.93–1.07)

0.9173

  Philippines

606

76.4

1.22 (1.15–1.30)

<.0001

  Thailand

514

61.2

0.98 (0.89–1.07)

0.6003

  Vietnam

348

39.8

0.57 (0.47–0.68)

<.0001

Male

 Taiwan

95777

82.4

1.00

 

 All migrant workers

963

65

0.76 (0.70–0.83)

<.0001

  Indonesia

180

98.8

1.18 (1.03–1.33)

0.0152

  Philippines

199

69.6

0.83 (0.69–0.97)

0.0170

  Thailand

407

61.8

0.71 (0.61–0.81)

<.0001

  Vietnam

176

49.7

0.50 (0.35–0.64)

<.0001

Female

 Taiwan

42643

37.3

1.00

 

 All migrant workers

1292

55.9

1.40 (1.35–1.46)

<.0001

  Indonesia

606

55.2

1.39 (1.31–1.47)

<.0001

  Philippines

407

71.9

1.66 (1.56–1.75)

<.0001

  Thailand

107

83.4

1.80 (1.62–1.99)

<.0001

  Vietnam

172

33.1

0.88 (0.73–1.03)

0.1145

aAverage Incidence was represented with annual cases per 105 persons in 10 years average

Poisson regression model was applied to test the differences among each group

The TB risk was highest in 45–54 year-old group (49.6 per 105) and lowest in ≤24 year-old group (12.4 per 105) in Taiwanese while the TB risk was highest in 25–34 year-old group (65.9 per 105) but lowest in 45–54 year-old group (30.8 per 105) in migrant workers in Table 4. Applying Poisson regression models to test the differences among Taiwanese and migrant workers in each age group, we found that the TB risk in migrant workers was 5.30-fold in ≤24 year-old group comparing with Taiwanese (95%CI: 4.83–5.83, P < 0.001). Compared with Taiwanese, the TB risk of migrant workers in 25–34 year old and 35–44 year old groups are 2.63 fold (95%CI: 2.49–2.79, P < 0.001) and 1.40 fold (95%CI: 1.27–1.54, P < 0.001) respectively.
Table 4

Comparison of TB incidence among migrant workers and Taiwanese, stratified by age group, 2004 to 2013

 

Tuberculosis Cases

Incidencea

Hazard ratio

P value

≤24 year-old

 Taiwanese

8862

12.4

1.00

 

 Migrant workers

457

65.9

5.30 (4.83–5.83)

<.0001

25–34 year-old

 Taiwanese

9631

25.2

1.00

 

 Migrant workers

1367

66.4

2.63 (2.49–2.79)

<.0001

35–44 year-old

 Taiwanese

12,203

32.7

1.00

 

 Migrant workers

427

45.7

1.40 (1.27–1.54)

<.0001

45–54 year-old

 Taiwanese

17,930

49.6

1.00

 

 Migrant workers

32

30.8

0.62 (0.44–0.88)

0.0071

aAverage Incidence was represented with annual cases per 105 persons in 10 years average

Poisson regression model was applied to test the differences among each group

Discussion

To our knowledge, this is the first study to explore the TB incidence of the migrant workers in Taiwan. The nationwide, long-term follow-up, retrospective cohort study investigated the absolute risk and relative risk of TB in Taiwanese and the migrant workers. Gated by pre-screening program, the TB incidence in migrant workers was similar to Taiwanese but much lower than their native countries. Stratified by gender and age, the highest TB incidence group of the migrant workers were young female, especial in the ≤24 year-old group. There were two hypotheses to explain the differences of TB incidence between Taiwanese and migrant workers.

First hypothesis was that we assumed the high TB incidence after arrival of migrant workers was contributed by reactivation of latent TB infection (LTBI) [7, 11, 20]. In previous studies, the migrant workers, the refugees and the immigrants of US and Europe posed a high TB incidence after their arrival because the most important risk factor of reactivation of LTBI was that they were from countries of high tuberculosis burden [6, 21]. Studies suggest that active TB will develop in 5 to 10% of persons with LTBI during their lifetimes [22]. And, the highest risk period of reactivation among migrant workers was within first year and then during 2 to 4 years after their arrival [23, 24]. Also, the highest and lowest TB incidence of migrant workers in Taiwan were from Philippines and Vietnam while their native countries were at highest and lowest TB burden, respectively. In line with previous studies, our findings implied that there was a parallel risk of reactivation of LTBI based on the TB prevalence of the native countries [6, 7]. The current screening tool, chest radiography, was sensitive to detect pulmonary active TB but insufficient to catch LTBI [1, 25]. Our study pointed out that there was still high TB incidence among migrant workers after their arrival within 30 months. It implied that the current routine chest radiography in migrant workers in Taiwan was for screening pulmonary reactivation of LTBI but not adequate for detecting LTBI [12].

The second hypothesis of the high TB incidence after arrival of migrant workers was due to a new TB infection in Taiwan. Inconsistent with previous findings, which LTBI was more in male and elderly [21, 26], our study revealed that there was more TB cases in female and young group. There are three types of migrant workers in Taiwan: (1) those who work for companies and factories are classified as industrial and business workers, (2) those who work at house unit for cooking, clothing and child raising are classified as household workers, and (3) those who work in health care facilities or respiratory care centers are classified as health care workers [27]. Most of the household workers and health care workers were young and female which frequently contacted with the elderly and the persons with chronic illness which were groups with high proportion of tuberculosis infection. In line with previous systematic review and meta-analysis, there is a higher burden of LTBI among health care workers than general population in high burden countries [28]. Also, the matched cohort study in Taiwan revealed that the health care workers were in an increased risk of active TB compared with general population [29]. Besides, in previous studies in US and China, a proportion of migrant workers lived in crowded and poor surroundings [30, 31] which might increase the ongoing transmission of TB from cases of reactivation of LTBI to TB naive persons nearby among migrant workers. Furthermore, migrant workers experienced more stress during their daily work [32] and was less accessible to medical services which make them more vulnerable to infectious diseases. Because we did not performed polymerase chain reaction and bacterial cultures in each case, the active TB of young female migrant workers could be resulted from LTBI or a new infection after close contacts of persons with tuberculosis [21]. No matter the high TB incidence of the migrant workers were from LTBI or a new infection, they were all active in social community and easily spread the Mycobacterium tuberculosis to the public. Because the migrant workers are accounted for approximately 2% of total population in Taiwan, it is important to review the current screening program of migrant workers to improve TB control.

In Taiwan, once the migrant workers were diagnosed with new active TB, they have to receive 14-days treatments and repatriate back to their native countries [12]. Also, the migrant workers with active TB would be suspended from their work and quickly process the repatriation. Since cultured-based laboratory results require 6-weeks to final report, the migrant workers have relatively low culture data [27]. Nevertheless, chest X-ray is a valid and cost-saving screening tool for active and old healed TB, and is widely used in countries with migrant workers from high-burden areas [33]. The problem is that chest X-ray for active TB screening poses an unneglectable risk of onward reactivation of LTBI when migrant workers come from high TB risk countries [7]. Therefore, adding a screening tool of LTBI for high risk group in migrant workers is one of the applicable approaches in the future.

There are several limitation in our study. First of all, this was a retrospective cohort study and subjects’ information was obtained from the registration of local health administrations. Although we extracted several important confounding factors including origin countries, age and genders of migrant workers, the impact of unobserved and unmeasurable confounding factors such as histories of close contact with TB and underlying diseases of migrant workers cannot be ruled out. Second, the TB diagnosis in this study was based on either culture positive or radiological manifestation which might be not reflect the true tuberculosis infection. And, the proportion of positive TB smear or culture among reported active TB in migrant workers was only one third in Taiwan [27]. Besides, the tuberculosis cases of Taiwanese population were not detected by active screening which might cause an underestimation in the TB incidence in Taiwan. Furthermore, because all migrant workers were seronegative of HIV before their entry and were excluded from the study once diagnosis of HIV infection, the HRs of TB incidence might be higher than our estimation between the migrant workers and Taiwanese. In Taiwan, HIV is also a notifiable disease by the Law on the Control of Communicable Diseases in Taiwan. The annual reported new cases of HIV in Taiwan were 6.7–9.6 /per 105. Due to the very low incidence of native HIV in Taiwan, we did not consider the problem of co- occurrence of TB and HIV [34].

However, this nationwide epidemiological investigation was consisted of whole population in Taiwan and all migrant workers from 2004 to 2013 which was representative and might provide a guide for further tuberculosis control in Taiwan.

Conclusions

In conclusion, we demonstrated that the female and young migrant workers from high TB incidence countries were as a key reservoir of tuberculosis with consequently reactivation of LTBI and a probable risk of ongoing transmission in the first few years after their arrival. Our findings implied that this risky group should be prioritized to screen for LTBI as well as active TB in pre-arrival and post-arrival program. Further investigation and culture-based studies were warranted.

Abbreviations

CIs: 

Confidence intervals

HRs: 

Hazard ratios

LTBI: 

Latent tuberculosis infection

NHI: 

National Health Insurance

TB: 

Tuberculosis

Declarations

Acknowledgements

We would like to thank Miss Chia-Chi Yu for her administrative assistance in the study.

Funding

This study has been partially sponsored by the Centers for Disease Control, Taiwan (YH10635).

Availability of data and materials

Please contact the authorship team to enquire regarding access to material.

Consent to participate

Not applicable; big data with individual de-identified detail.

Authors’ contributions

CWL was responsible for the data analysis and interpretation, and drafting and editing of the paper. KCH contributed to the study’s conception, initiation and design, the interpretation of the results, and editing of the paper. All authors reviewed and approved the final submission.

Ethics approval and consent to participate

The design of the study was approved by the Research Ethics Committee in National Taiwan University Hospital in Taiwan (201807018W) before the study was conducted.

Consent for publication

Written informed consent was not obtained from the participant for publication because of the individual de-identified details in original row data.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
Department of Family Medicine, National Taiwan University Hospital, Taipei, Taiwan
(2)
Department of Family Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan
(3)
Department of Family Medicine, National Taiwan University Hospital Bei-Hu Branch, Taipei, Taiwan
(4)
Centers for Disease Control, Taipei, Taiwan
(5)
Department of Medical Education, National Taiwan University Hospital, Taipei, Taiwan

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