Associations between Diabetes Mellitus and Nontuberculous Mycobacterium-Caused Diseases in Taiwan: A Nationwide Cohort Study

Jui-Yang Wang Department of Family Medicine, Tri-Service General Hospital SongShan Branch, National Defense Medical Center, Taipei City, Taiwan;
Department of Health Promotion and Health Education, National Taiwan Normal University, Taipei City, Taiwan;

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Hsin-Chung Lin Division of Clinical Pathology, Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei City, Taiwan;

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Hsin-An Lin Division of Infection, Department of Medicine, Tri-Service General Hospital SongShan Branch, National Defense Medical Center, Taipei City, Taiwan;

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Chi-Hsiang Chung School of Public Health, National Defense Medical Center, Taipei City, Taiwan;
Taiwanese Injury Prevention and Safety Promotion Association, Taipei City, Taiwan;

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Lih-Chyang Chen Department of Medicine, Mackay Medical College, New Taipei City, Taiwan;

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Kuo-Yang Huang Graduate Institute of Pathology and Parasitology, National Defense Medical Center, Taipei City, Taiwan;

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Chien-An Sun Department of Public Health, College of Medicine, Fu-Jen Catholic University, New Taipei City, Taiwan;
Big Data Research Center, College of Medicine, Fu-Jen Catholic University, New Taipei City, Taiwan;

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Wu-Chien Chien School of Public Health, National Defense Medical Center, Taipei City, Taiwan;
Taiwanese Injury Prevention and Safety Promotion Association, Taipei City, Taiwan;
Department of Medical Research, Tri-Service General Hospital, National Defense Medical Center, Taipei City, Taiwan;
Graduate Institute of Life Sciences, National Defense Medical Center, Taipei City, Taiwan

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Jong-Long Guo Department of Health Promotion and Health Education, National Taiwan Normal University, Taipei City, Taiwan;

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ABSTRACT.

Patients with diabetes mellitus (DM) are at greater risk of developing active tuberculosis and other intracellular bacterial infections, although the risk of acquiring infections from nontuberculous Mycobacterium (NTM) remains undefined. This study evaluated associations between DM and incidence of NTM infection-caused pulmonary and cutaneous diseases. Data for DM patients were extracted from the National Health Insurance Research Database of Taiwan. The DM cohort included 136,736 patients, and cases were matched randomly by age, gender, and index year with non-DM patients. Multivariate Cox proportional hazards regression was used to calculate adjusted hazard ratios of incident NTM-caused diseases in the DM cohort compared with non-DM control subjects. The frequency of incident NTM-caused diseases was significantly greater in DM patients (0.12%) than in non-DM patients (0.08%) (P < 0.05), including patients with type 1 DM (0.12%) and type 2 DM (0.12%) (all P < 0.05). Adjusted multivariate Cox regression analysis revealed that the incidence of NTM-caused diseases in DM patients was 1.43-fold greater than that in non-DM patients overall (P < 0.05), particularly in pulmonary (1.13-fold), other specific (excluding pulmonary, cutaneous, and disseminated diseases; 3.88-fold), and unspecific (atypical NTM infection; 1.54-fold) diseases (all P < 0.05). In conclusion, both type 1 DM and type 2 DM patients have high risk of NTM-caused diseases, suggesting that physicians need to pay more attention to this issue concerning the high risk of NTM-caused infection in DM patients.

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Author Notes

Address correspondence to Wu-Chien Chien, Department of Medical Research, Tri-Service General Hospital, National Defense Medical Center, No. 325, Section 2, Cheng-Kung Road, Neihu District, Taipei City, 11490, Taiwan, E-mail: chienwu@ndmctsgh.edu.tw or Jong-Long Guo, Department of Health Promotion and Health Education, National Taiwan Normal University, No. 162, Section 1, Heping E. Road, Taipei City 106, Taiwan, E-mail: jonglong@ntnu.edu.tw.

Financial support: This work was supported by the Tri-Service General Hospital Songshan Branch, Taiwan (TSGH-SSD-108018) to J.-Y.W., and the Tri-Service General Hospital, Taiwan (TSGH-B-109010 and TSGH-B-110012) to W.-C.C and (TSGH-D-110098) to HCL, and Ministry of National Defense Medical Affairs Bureau, Taiwan (MND-MAB-110-110) to HCL.

Authors’ addresses: Jui-Yang Wang, Department of Family Medicine, Tri-Service General Hospital SongShan Branch, National Defense Medical Center, Taipei City, Taiwan, and Department of Health Promotion and Health Education, National Taiwan Normal University, Taipei City, Taiwan, E-mail: garywawa@yahoo.com.tw. Hsin-Chung Lin, Division of Clinical Pathology, Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei City, Taiwan, E-mail: hsinchunglin@gmail.com. Hsin-An Lin, Division of Infection, Department of Medicine, Tri-Service General Hospital SongShan Branch, National Defense Medical Center, Taipei City, Taiwan, E-mail: shinean0928@gmail.com. Chi-Hsiang Chung, School of Public Health, National Defense Medical Center, Taipei City, Taiwan, and Taiwanese Injury Prevention and Safety Promotion Association, Taipei City, Taiwan, E-mail: g694810042@gmail.com. Lih-Chyang Chen, Department of Medicine, Mackay Medical College, New Taipei City, Taiwan, E-mail: lihchyang@mmc.edu.tw. Kuo-Yang Huang, Graduate Institute of Pathology and Parasitology, National Defense Medical Center, Taipei City, Taiwan, E-mail: cguhgy6934@gmail.com. Chien-An Sun, Department of Public Health, College of Medicine, Fu-Jen Catholic University, New Taipei City, Taiwan, and Big Data Research Center, College of Medicine, Fu-Jen Catholic University, New Taipei City, Taiwan, E-mail: 040866@mail.fju.edu.tw. Wu-Chien Chien, School of Public Health, National Defense Medical Center, Taipei City, Taiwan, Taiwanese Injury Prevention and Safety Promotion Association, Taipei City, Taiwan, Department of Medical Research, Tri-Service General Hospital, National Defense Medical Center, Taipei City, Taiwan, and Graduate Institute of Life Sciences, National Defense Medical Center, Taipei City, Taiwan, E-mail: chienwu@ndmctsgh.edu.tw. Jong-Long Guo, Department of Health Promotion and Health Education, National Taiwan Normal University, Taipei City, Taiwan, E-mail: jonglong@ntnu.edu.tw.

  • 1.

    Baker RG, Hayden MS, Ghosh S, 2011. NF-kappaB, inflammation, and metabolic disease. Cell Metab 13: 11–22.

  • 2.

    Viswanathan V, Vigneswari A, Selvan K, Satyavani K, Rajeswari R, Kapur A, 2014. Effect of diabetes on treatment outcome of smear-positive pulmonary tuberculosis: a report from South India. J Diabetes Complications 28: 162–165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Bridson T, Matthiesson A, Owens L, Govan B, Norton R, Ketheesan N, 2015. Diabetes: a contributor to tuberculosis in tropical Australia. Am J Trop Med Hyg 93: 547–548.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Lin YH, Chen CP, Chen PY, Huang JC, Ho C, Weng HH, Tsai YH, Peng YS, 2015. Screening for pulmonary tuberculosis in type 2 diabetes elderly: a cross-sectional study in a community hospital. BMC Public Health 15: 3.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Kumar Nathella P, Babu S, 2017. Influence of diabetes mellitus on immunity to human tuberculosis. Immunology 152: 13–24.

  • 6.

    WHO , 2017. World Health Organization (WHO): Global Tuberculosis Report 2017. Geneva, Switzerland: World Healther Organization. Available at: https://www.who.int/tb/publications/global_report/en/. Accessed September 8, 2021.

    • PubMed
    • Export Citation
  • 7.

    Vaerewijck MJ, Huys G, Palomino JC, Swings J, Portaels F, 2005. Mycobacteria in drinking water distribution systems: ecology and significance for human health. FEMS Microbiol Rev 29: 911–934.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Chan ED, Iseman MD, 2013. Underlying host risk factors for nontuberculous mycobacterial lung disease. Semin Respir Crit Care Med 34: 110–123.

  • 9.

    Winthrop KL, McNelley E, Kendall B, Marshall-Olson A, Morris C, Cassidy M, Saulson A, Hedberg K, 2010. Pulmonary nontuberculous mycobacterial disease prevalence and clinical features: an emerging public health disease. Am J Respir Crit Care Med 182: 977–982.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Hodgson KA, Morris JL, Feterl ML, Govan BL, Ketheesan N, 2011. Altered macrophage function is associated with severe Burkholderia pseudomallei infection in a murine model of type 2 diabetes. Microbes Infect 13: 1177–1184.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Orme IM, Ordway DJ, 2014. Host response to nontuberculous mycobacterial infections of current clinical importance. Infect Immunol 82: 3516–3522.

  • 12.

    Drummond WK, Kasperbauer SH, 2019. Nontuberculous mycobacteria: epidemiology and the impact on pulmonary and cardiac disease. Thorac Surg Clin 29: 59–64.

  • 13.

    Hoefsloot W et al., 2013. The geographic diversity of nontuberculous mycobacteria isolated from pulmonary samples: an NTM-NET collaborative study. Eur Respir J 42: 1604–1613.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Jackson E, Stewart A, Maguire EJ, Norton RE, 2007. Mycobacterial soft tissue infections in North Queensland. ANZ J Surg 77: 368–370.

  • 15.

    Song JW, Koh WJ, Lee KS, Lee JY, Chung MJ, Kim TS, Kwon OJ, 2008. High-resolution CT findings of Mycobacterium avium intracellulare complex pulmonary disease: correlation with pulmonary function test results. AJR Am J Roentgenol 191: W160–W166.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Jeong YJ, Lee KS, Koh WJ, Han J, Kim TS, Kwon OJ, 2004. Nontuberculous mycobacterial pulmonary infection in immunocompetent patients: comparison of thin-section CT and histopathologic findings. Radiology 231: 880–886.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Fjallbrant H, Akerstrom M, Svensson E, Andersson E, 2013. Hot tub lung: an occupational hazard. Eur Respir Rev 22: 88–90.

  • 18.

    Ding LW, Lai CC, Lee LN, Hsueh PR, 2006. Disease caused by non-tuberculous mycobacteria in a university hospital in Taiwan, 1997–2003. Epidemiol Infect 134: 1060–1067.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Yeh JJ, Wang YC, Sung FC, Chou CY, Kao CH, 2014. Nontuberculosis Mycobacterium disease is a risk factor for chronic obstructive pulmonary disease: a nationwide cohort study. Lung 192: 403–411.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Oh TH, Kim UJ, Kang SJ, Jang HC, Park KH, Jung SI, Ahn JH, 2018. Disseminated invasive Mycobacterium marinum infection involving the lung of a patient with diabetes mellitus. Infect Chemother 50: 59–64.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    National Health Insurance Administration , 2020. Universal Health Coverage in Taiwan. Available at: https://www.nhi.gov.tw/english/Content_List.aspx?n=8FC0974BBFEFA56D&topn=ED4A30E51A609E49. Accessed September 8, 2021.

    • PubMed
    • Export Citation
  • 22.

    American Thoracic Society , 1997. Diagnosis and treatment of disease caused by nontuberculous mycobacteria. Am J Respir Crit Care Med 156: S1–S25.

  • 23.

    Zhang ZX, Cherng BPZ, Sng LH, Tan YE, 2019. Clinical and microbiological characteristics of non-tuberculous mycobacteria diseases in Singapore with a focus on pulmonary disease, 2012–2016. BMC Infect Dis 19: 436.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Deyo RA, Cherkin DC, Ciol MA, 1992. Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45: 613–619.

  • 25.

    Adjemian J, Olivier KN, Seitz AE, Holland SM, Prevots DR, 2012. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries. Am J Respir Crit Care Med 185: 881–886.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Brode SK, Marchand-Austin A, Jamieson FB, Marras TK, 2017. Pulmonary versus nonpulmonary nontuberculous mycobacteria, Ontario, Canada. Emerg Infect Dis 23: 1898–1901.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Huang HL, Cheng MH, Lu PL, Shu CC, Wang JY, Wang JT, Chong IW, Lee LN, 2017. Epidemiology and predictors of NTM pulmonary infection in Taiwan: a retrospective, five-year multicenter study. Sci Rep 7: 16300.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Koh WJ, Kwon OJ, Lee KS, 2005. Diagnosis and treatment of nontuberculous mycobacterial pulmonary diseases: a Korean perspective. J Korean Med Sci 20: 913–925.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Lim AYH, Chotirmall SH, Fok ETK, Verma A, De PP, Goh SK, Puah SH, Goh DEL, Abisheganaden JA, 2018. Profiling non-tuberculous mycobacteria in an Asian setting: characteristics and clinical outcomes of hospitalized patients in Singapore. BMC Pulm Med 18: 85.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Lim HJ, Park CM, Park YS, Lee J, Lee SM, Yang SC, Yoo CG, Kim YW, Han SK, Yim JJ, 2011. Isolation of multiple nontuberculous mycobacteria species in the same patients. Int J Infect Dis 15: e795–e798.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Luthra S, Rominski A, Sander P, 2018. The role of antibiotic-target-modifying and antibiotic-modifying enzymes in Mycobacterium abscessus drug resistance. Front Microbiol 9: 2179.

    • PubMed
    • Search Google Scholar
    • Export Citation
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