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 Table of Contents  
ARTICLE
Year : 2016  |  Volume : 5  |  Issue : 2  |  Page : 170-176

Impact of industrial structure and soil exposure on the regional variations in pulmonary nontuberculous mycobacterial disease prevalence


1 Department of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
2 Department of Respiratory Medicine, Allergy and Clinical Immunology, Nagoya City University School of Medical Sciences, Nagoya, Japan
3 Department of Respiratory Medicine, National Hospital Organization Kyoto Medical Center, Kyoto, Japan
4 Department of Respiratory Medicine, Takeda General Hospital, Kyoto, Japan
5 Department of Cardiovascular Medicine, Ako City Hospital, Ako, Japan
6 Department of Gastroenterology and Hepatology, Ako City Hospital, Ako, Japan
7 Department of Respiratory Medicine, Kyoto Katsura Hospital, Kyoto, Japan
8 Department of Laboratory Medicine, Kyoto City Hospital, Kyoto, Japan
9 Department of Clinical Laboratory, University Hospital, Kyoto Prefectural University of Medicine, Kyoto, Japan
10 Department of Infection Control and Clinical Laboratory, Kyoto Prefectural University of Medicine, Kyoto, Japan
11 Clinical Laboratory of Medicine, Kyoto University, Kyoto, Japan
12 Department of Respiratory Care and Sleep Control Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan

Date of Web Publication9-Feb-2017

Correspondence Address:
Yutaka Ito
Department of Respiratory Medicine, Allergy and Clinical Immunology, Nagoya City University School of Medical Sciences, 1 Kawasumi, Mizuho-cho, Mizuho-ku, Nagoya 467-8601
Japan
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Source of Support: None, Conflict of Interest: None


DOI: 10.1016/j.ijmyco.2016.02.006

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  Abstract 

Objective/background: The prevalence of pulmonary nontuberculous mycobacterial (pNTM) disease, including Mycobacterium avium complex (MAC), varies widely according to geographic region. However, the factors that influence regional variations in pNTM disease prevalence remain unknown. This study was undertaken to examine whether environmental or occupational factors or host traits could influence regional variations in pNTM disease prevalence.
Methods: We collected laboratory data on pulmonary tuberculosis (pTB) and pNTM from two hospitals in the West Harima area of Japan and five hospitals in Kyoto City, Japan from 2012 to 2013. We estimated microbiological pNTM disease prevalence by multiplying all pTB cases in each area with the ratio of pNTM cases and pTB cases at the survey hospitals in each area. We administered a standardized questionnaire to 52 patients and 120 patients with pulmonary MAC (pMAC) disease at Ako City Hospital and Kyoto University Hospital, respectively.
Results: The estimated prevalence of microbiological pNTM disease in the West Harima area (85.4/100,000 population-years) was significantly higher than that observed in Kyoto City (23.6/100,000 population-years; p < .001). According to multiple logistic regression analysis, in Ako City Hospital, primary (activities directly related to natural resources) and secondary industries (construction, mining, and manufacturing primary industry produce; odds ratio [OR] = 4.79; 95% confidence interval [CI] = 1.49−14.0; p = .007) and soil exposure (OR = 13.6; 95% CI = 4.94−45.26; p < .001) were associated with pMAC disease.
Conclusion: Environmental factors, both industrial structures associated with occupational dust and environmental soil exposure, could influence the regional variations in pNTM disease prevalence.

Keywords: Environmental factors, Host factors, Mycobacterium avium complex, Nontuberculous mycobacteria, Prevalence


How to cite this article:
Hamada S, Ito Y, Hirai T, Murase K, Tsuji T, Fujita K, Mio T, Maekawa K, Fujii T, Ono S, Nishimura T, Hayashi A, Komori T, Fujita N, Niimi A, Ichiyama S, Chin K, Mishima M. Impact of industrial structure and soil exposure on the regional variations in pulmonary nontuberculous mycobacterial disease prevalence. Int J Mycobacteriol 2016;5:170-6

How to cite this URL:
Hamada S, Ito Y, Hirai T, Murase K, Tsuji T, Fujita K, Mio T, Maekawa K, Fujii T, Ono S, Nishimura T, Hayashi A, Komori T, Fujita N, Niimi A, Ichiyama S, Chin K, Mishima M. Impact of industrial structure and soil exposure on the regional variations in pulmonary nontuberculous mycobacterial disease prevalence. Int J Mycobacteriol [serial online] 2016 [cited 2022 Jun 30];5:170-6. Available from: https://www.ijmyco.org/text.asp?2016/5/2/170/199926


  Introduction Top


Pulmonary nontuberculous mycobacterial (pNTM) disease is recognized because of its increasing prevalence, particularly in developed countries [1]. Recently, in Japan, Morimoto et al. [2] estimated pNTM disease prevalence to be 33–65/100,000 population-years.

NTM species, including Mycobacterium avium complex (MAC), are broadly observed in the environment, particularly in aerosols generated from colonized soil and water [3]. Therefore, the risk of acquiring pNTM disease is associated with environmental factors, including climate and soil characteristics and the engagement in aerosol-generating occupations (e.g., agriculture and construction works) and other activities [4],[5],[6],[7],[8],[9],[10],[11],[12]. Furthermore, the risk of acquiring pNTM disease is also associated with host factors (e.g., racial differences, female gender, advanced age, skeletal abnormalities, underlying diseases, and the use of inhaled corticosteroid and immunomodulatory drugs) [13],[14],[15],[16].

pNTM disease prevalence varies widely according to the geographic region. Some reports showed that the regional variations in pNTM disease prevalence were correlated with host factors, both race and income, while others revealed that they were associated with environmental factors, both climate and soil characteristics. Therefore, whether environmental or host factors can influence the regional variations in pNTM disease prevalence remains unknown [17],[18],[19],[20],[21]. Furthermore, the effects of other host (e.g., underlying diseases and medications) and environmental factors (e.g., occupations and frequency of exposure to soil and water) on regional variations in pNTM disease prevalence have not been investigated.

In this study, we first examined pNTM disease prevalence in the West Harima area (rural area with a small population) and Kyoto City (urban area with a large population) in Japan. Here, we estimated pNTM disease prevalence in each area by the correction with numbers of pulmonary tuberculosis (pTB) patients according to previous reports [22],[23]. Next, using clinical data and a questionnaire, we examined whether environmental and host factors could influence the regional variations in pNTM disease prevalence.


  Materials and methods Top


Study area

The population of West Harima area, including Ako city, Aioi City, and Ako County, was 96,489 in 2012 and 95,527 in 2013. The population in Kyoto City was 1,473,069 in 2012 and 1,470,730 in 2013. The West Harima area has a Seto Inland Sea climate, which is observed around the region of the Seto Inland Sea, and a mild and sunny climate characterized by low rainfall in August. The annual precipitation, mean humidity, and mean maximal and minimal temperatures in the West Harima area are approximately 1200 mm, 71%, 20.2°C, and 10.8°C, respectively. Kyoto City has both a Seto Inland Sea climate and inland climate, as typified by a hot summer and cold winter. The annual precipitation, mean humidity, and mean maximal and minimal temperatures of Kyoto City are approximately 1500 mm, 71%, 20.8°C, and 11.7°C, respectively.

Industrial structure

We divided the industrial structure into three categories based on the national census as follows: primary industry (activities directly related to natural resources, e.g., agriculture, forestry, and fishery); secondary industry (construction, mining, and manufacturing industry product); and tertiary industry (services) [24]. The results of a national census taken in 2010 revealed that in the West Harima area, 2.1%, 34.6%, and 63.3% of the population was engaged in primary, secondary, and tertiary industries as compared to 0.9%, 21.7%, and 77.5%, respectively, in Kyoto City [24].

Data collection

We collected microbiological data for all culture-positive acid-fast bacilli to examine the numbers of patients with pNTM disease who met the American Thoracic Society microbiological criteria (microbiological pNTM disease) [25] from two local hospitals [Ako City Hospital (396 beds) and Ako Central Hospital (265 beds)] in the West Harima area and five medical centers [Kyoto University Hospital (1121 beds), University Hospital, Kyoto Prefectural University of Medicine (1065 beds), Kyoto Katsura Hospital (585 beds), Kyoto City Hospital (548 beds), and National Hospital Organization Kyoto Medical Center (600 beds)] in Kyoto City from 2012 to 2013. In Japan, every diagnosed case of TB was reported by a clinician to the local public health office, because notification of TB cases is mandatory. Data for all culture-positive pTB cases were obtained from each public health office in the West Harima area and Kyoto City, respectively. Isolates that could not be discriminated between M. avium and M. intracellulare were designated as unspecified MAC.

We also examined the characteristics of patients with pulmonary MAC (pMAC) disease in the West Harima area and Kyoto City. In total, 52 patients with pMAC disease who lived in Ako city or Ako County were followed at Ako City Hospital between January 2012 and November 2013, and 120 patients with pMAC disease who lived in Kyoto City were followed at Kyoto University Hospital over the same period. Ako City Hospital and Kyoto University Hospital are the local central hospitals in each area. The diagnosis of pMAC disease was based on the ATS criteria [25]. Clinical data, including demographic characteristics, the presence of underlying diseases and conditions, and the microbiological results for respiratory specimens, were collected from clinical records. All participants completed a standardized questionnaire that included questions about their experiences, such as occupations, soil exposure from farming or gardening, and water exposure from taking baths, showering, hot tub use, washing dishes, or swimming in a pool [4],[5]. High soil exposure was defined as ≥2h/wk of soil-related activities. Chest radiographs and computed tomography (CT) scans were reviewed by two pulmonary clinicians. The review board of Kyoto University Hospital approved the research protocol (E1773 and E1905).

Estimated prevalence of microbiological pNTM disease

To estimate microbiological pNTM disease prevalence, we used the following equation according to previous reports [22],[23]:

X × Z/Y = P, (1)

where X is the incidence of culture-positive pTB (per 100,000 population-years) in each area, Y is the number of patients diagnosed with culture-positive pTB at the survey hospitals in each area, Z is the number of patients with microbiological pNTM disease at the survey hospitals in each area, and P is the estimated prevalence of microbiological pNTM disease in each area.

2.5 Statistical analysis

To determine which variables could determine the regional variations in pNTM disease prevalence, we first compared the characteristics of patients with pMAC disease between the West Harima area and Kyoto City. Categorical and continuous variables were compared using the chi-square test and Wilcoxon's test, respectively, followed by multiple logistic regression analysis. The variables entered in the multivariate analysis were those yielding a p < .05 on univariate analysis. A p < .05 was considered significant. All statistical analyses were performed using JMP 10 software (SAS Institute Inc., Cary, NC, USA).


  Results Top


3.1 Estimated prevalence of microbiological pNTM disease

[Table 1] describes the estimated prevalence of microbiological pNTM disease in the West Harima area and Kyoto City. The numbers of culture-positive pTB cases registered in each public health office from 2012 to 2013 were 32 and 568 in the West Harima area and Kyoto City, respectively. The incidences of culture-positive pTB in the West Harima area and Kyoto City were 16.7/100,000 population-years and 19.3/100,000 population-years, respectively. The numbers of patients with culture-positive pTB recorded the hospitals in the West Harima area and Kyoto City were 9 (7 in Ako City Hospital and 2 in Ako Central Hospital) and 203 (82 in Kyoto University Hospital, 7 in University Hospital, Kyoto Prefectural University of Medicine, 10 in Kyoto-Katsura Hospital, 82 in Kyoto City Hospital, and 22 in National Hospital Organization Kyoto Medical Center), respectively. The numbers of patients with microbiological pNTM disease in the West Harima area and Kyoto City were 46 (45 in Ako City Hospital and 1 in Ako Central Hospital) and 248 (147 in Kyoto University Hospital, 1 in University Hospital, Kyoto Prefectural University of Medicine, 47 in Kyoto-Katsura Hospital, 36 in Kyoto City Hospital, and 17 in National Hospital Organization Kyoto Medical Center), respectively. Using Eq. (1), the estimated prevalence of microbiological pNTM disease in the West Harima area (85.4/100,000 population-years) was significantly higher than that in Kyoto City (23.6/100,000 population-years; p < .001).
Table 1: Estimated prevalence of microbiological pulmonary nontuberculous mycobacterial disease in the West Harima area and Kyoto City in Japan from 2012 to 2013.

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Patients diagnosed with microbiological pNTM disease in the West Harima area were more elderly compared with those in Kyoto City (74.6±9.6years vs. 70.2±9.3years; p = .011). In both areas, female gender predominated (71.7% in West Harima area and 65.7% in Kyoto City). The diagnostic sources in the West Harima area were sputum, specimens obtained through bronchoscopy, and lung tissue in 44 patients, 2 patients, and 0 patients, versus 212 patients, 31 patients, and 5 patients, respectively, in Kyoto City. In the West Harima area and Kyoto City, MAC accounted for >90% of NTM species (91.3% and 91.8%, respectively), followed by M. abscessus (4.4% and 3.6%, respectively), and M. kansasii (2.2% and 3.2%, respectively; [Figure 1]).
Figure 1: Species distribution in patients with microbiological pulmonary nontuberculous mycobacterial disease. In both the West-Harima area and Kyoto City in Japan, Mycobacterium avium complex accounted for >90% of nontuberculous mycobacterial species. Note. M, Mycobacterium; MAC, Mycobacterium avium complex. aIsolates that could not be discriminated between M. avium and M. intracellulare were designated as Unspecified MAC.

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3.2 Characteristics of patients with pMAC disease

The characteristics of patients with pMAC disease in Ako City Hospital and Kyoto University Hospital are shown in [Table 2]. Patients in Ako City Hospital tended to be older than those in Kyoto University Hospital (67.0±8.8years vs. 63.2±9.9years; p = .051). In both hospitals, there were no differences in body shape, and female gender predominated. Regarding CT findings, in Kyoto University Hospital, a cavitary form was found to be more frequent than that observed at Ako City Hospital (25.8% vs. 9.6%; p = .016).
Table 2: Clinical data of the patients with pulmonary Mycobacterium avium complex disease in Ako City Hospital and Kyoto University Hospital in Japan.

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Environmental exposure and industrial structures for patients with pMAC disease in Ako City Hospital and Kyoto University Hospital are presented in [Table 3]. More patients in Ako City Hospital experienced high soil exposure (≥2h/wk) as compared to those in Kyoto University Hospital (63.5% vs. 23.3%; p < .001). Concerning the source of soil exposure, in Ako City Hospital, farming was a more frequent source of exposure than that observed in Kyoto University Hospital (36.5% vs. 8.3%; p < .001). Regarding water exposure, patients in Kyoto University Hospital used showers more frequently than those in Ako City Hospital (66.7% vs. 15.4%; p < .001). More patients with pMAC disease in Ako City Hospital were engaged in primary (9.6% vs. 0.8%; p = .004) and secondary industries (32.7% vs. 10.8%; p =.005) than those observed in Kyoto University Hospital.
Table 3: Environmental exposure and industrial structures in patients with pulmonary Mycobacterium avium complex disease in Ako City Hospital and Kyoto University Hospital in Japan.

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By multiple logistic regression analysis, we determined that primary and secondary industries (odds ratios [OR] = 4.79; 95% confidence interval [CI] = 1.49−14.0; p = .007) and high soil exposure (OR = 13.6; 95% CI = 4.94−45.26; p < .001) were associated with pMAC disease in Ako City Hospital ([Table 4]).
Table 4: Factors associated with pulmonary Mycobacterium avium complex disease in Ako City Hospital in Japan.

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  Discussion Top


We revealed that the estimated prevalence of microbiological pNTM disease was significantly higher in the West Harima area than in Kyoto City. This difference was influenced by the engagement in industries associated with occupational dust and experience of high soil exposure (≥2h/wk). To our knowledge, this is the first report revealing the impact of occupations and frequencies exposed to soil and water on the regional variations in pNTM disease prevalence using a questionnaire.

In this study, we first revealed that environmental factors, both the industrial structure with a high rate of primary and secondary industries and frequencies exposed to soil, but not host factors, were associated with regional variations in pNTM disease prevalence. Previous reports showed that regional variations in pNTM disease prevalence were associated with environmental factors, both climate (e.g., high moisture) and soil characteristics [19],[20]. Concerning the associations of industry with pNTM infections, Reed et al. [11] reported that occupations involving prolonged soil exposure (e.g., farming) increased the risk of pMAC infection [11]. Additionally, tunnel work and mining, including dusty jobs involving silica dust inhalation, increase the risk of pNTM disease [26],[27]. Concerning the associations of soil exposure with pNTM infections, we reported that environmental soil exposure was an independent risk factor for pMAC disease and the development of polyclonal and mixed MAC infections [4],[6],[7]. Additionally, we reported that low soil exposure was associated with better microbiological outcomes in patients with pMAC disease [5].

We estimated pNTM disease prevalence in each area by correction with numbers of pTB patients according to previous reports [23],[25], because it is difficult to determine the precise prevalence of pNTM disease. In this study, the estimated prevalence of microbiological pNTM disease in the West Harima area and Kyoto City was 85.4/100,000 population-years and 23.6/100,000 population-years, respectively. The overall prevalence in the two areas was 26.5/100,000 population-years. Recently, Morimoto et al. [2] reported that pNTM disease prevalence calculated from mortality rates ranged from 33–65/100,000 population-years in Japan [2]. In North America, Europe, Australia, and other Asian countries than Japan, previous studies reported that pNTM disease prevalence ranged from 3 population-years to 14.1/100,000 population-years [28],[29],[30],[31],[32],[33],[34]. In Japan, pNTM disease prevalence was suspected to be higher than that in most other countries.

This study had some limitations. First, we evaluated only two areas, namely the West Harima area and Kyoto City. Second, we only identified nine patients with culture-positive pTB in the West Harima area from 2012 to 2013, whereas the public health office in this area reported 32 patients. Third, in the West Harima area, more people engaged in primary and secondary industries as compared to Kyoto City (2.1% vs. 0.9% and 34.6% vs. 21.7%, respectively) [24]. Therefore, this industrial background could have influenced our results. Future studies comprising many regions having similar industrial structures are needed. Finally, we conducted a questionnaire survey at only one hospital each in the West Harima area (Ako City Hospital) and Kyoto City (Kyoto University Hospital). Each hospital covered more than half of the patients with microbiological NTM disease in this study; particularly, Ako City Hospital and Kyoto University Hospital covered 97.8% and 59.3%, respectively, of the patients with microbiological NTM disease. However, it is possible that the clinical data obtained for each area does not reflect the characteristics of the entire region.


  Conclusion Top


We concluded that environmental factors, both industrial structures associated with occupational dust and environmental soil exposure, could influence the regional variations in pNTM disease prevalence. Future studies comprising many regions and hospitals are needed to reveal the effect of industrial structure on the regional prevalence of pNTM disease.


  Conflicts of interest Top


All authors declare no conflicts of interest regarding to this report.





The authors thank Ms. Emi Okamura, Ms. Hiroyo Takahata, and Ms. Mikako Okeguchi for collecting microbiological data of all culture-positive acid-fast bacilli from Kyoto Katsura Hospital, Ako City Hospital, and Ako Central Hospital, respectively. The authors also thank Ms. Noriko Fujita for helping Ms. Emi Okamura with collecting microbiological data in Kyoto Katsura Hospital. The Department of Respiratory Care and Sleep Control Medicine is funded by endowments from Philips-Respironics, Teijin Pharma, Fukuda Denshi, and Fukuda Lifetec Keiji to Kyoto University.



 
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    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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