Skip to main content

Advertisement

SpringerLink
Log in

Isolation and identification of nontuberculous mycobacteria from hospitalized patients and drinking water samples—examination of their correlation by chemometrics

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Nontuberculous mycobacteria (NTM) have been found to be widely dispersed in the environment and are being considered potentially pathogenic for humans and animals, while reports of their human to human transmission are absent. Water and aerosols are potential transmission modes of NTM to humans. Hospitalized patients with NTM infections were studied together with drinking water samples from their respective residence areas during 2003–2013. Cluster analysis and factor analysis were used to analyze the data matrix. A total of 367 hospitalized patients living in 30 localities in the Prefecture of Larissa were tested positive for NTM. The most frequently isolated NTM species of the 383 NTM isolates from the clinical specimens were Mycobacterium fortuitum (n = 118, 30.8 %), M. gordonae (n = 87, 22.7 %), M. peregrinum (n = 46, 12.0 %), M. chelonae (n = 11, 2.9 %), M. avium (n = 8, 2.1 %), and M. intracellulare (n = 7, 1.8 %), while 88 (23.0 %) of these isolates were not identified. It is noted that in 8 patients, M. tuberculosis was isolated simultaneously with one NTM, in 15 patients, together with two types of NTM, while in 1 patient, it was found at the same time as three different NTM. In addition, 3360 drinking water samples were collected from 30 localities and analyzed during 2010 to 2013; they were found 11.2 % NTM positive. Cluster analysis and factor analysis results confirm that NTM strains are correlated to each other in both isolated samples from patients and drinking water, while the strength of their correlation varied from weak to moderate (e.g., factor loadings ranged from 0.69 to 0.74 when all data are considered). These results provide indications that drinking water could be linked with NTM cases in humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Archibald, L. K., & Jarvis, W. R. (2011). Health care-associated infection outbreak investigations by the centers for disease control and prevention, 1946–2005. American Journal of Epidemiology, 174, S47–S64.

    Article  Google Scholar 

  • Biet, F., & Boschiroli, M. L. (2014). Non-tuberculous mycobacterial infections of veterinary relevance. Research in Veterinary Science, 97, S69–S77. doi:10.1016/j.rvsc.2014.08.007.

    Article  Google Scholar 

  • Billinger, M. E., Olivier, K. N., Viboud, C., Montes de Oca, R., Steiner, C., Holland, S. M., & Prevots, D. R. (2009). Nontuberculous mycobacteria-associated lung disease in hospitalized persons, United States, 1998–2005. Emerging Infectious Diseases, 15(10), 1562–1569.

    Article  Google Scholar 

  • Briancesco, R., Semproni, M., Libera, D., Sdanganelli, M., & Bonadonna, L. (2010). Non-tuberculous mycobacteria and microbial populations in drinking water distribution systems. Annali dell’Istituto Superiore di Sanità, 46(3), 254–258.

    CAS  Google Scholar 

  • Castillo-Rodal, A. I., Mazari-Hiriart, M., Lloret-Sánchez, L. T., Sachman-Ruiz, B., Vinuesa, P., & López-Vidal, Y. (2012). Potentially pathogenic nontuberculous mycobacteria found in aquatic systems. Analysis from a reclaimed water and water distribution system in Mexico City. European Journal of Clinical Microbiology & Infectious Diseases, 31, 683–694.

    Article  CAS  Google Scholar 

  • Chou, M. P., Clements, A. C. A., & Thomson, R. M. (2014). A spatial epidemiological analysis of nontuberculous mycobacteria infections in Queensland, Australia. BMC Infectious Diseases, 14, 279.

    Article  Google Scholar 

  • Cook, J. L. (2010). Nontuberculous mycobacteria: opportunistic environmental pathogens for predisposed hosts. British Medical Bulletin, 96, 45–59.

    Article  Google Scholar 

  • Dantec, C. L., Duguet, J. P., Montiel, A., Dumoutier, N., Dubrou, S., & Vincent, V. (2002). Occurrence of mycobacteria in water treatment lines and in water distribution systems. Applied and Emvironmental Microbiology, 68(11), 5318–5325.

    Article  Google Scholar 

  • Dirac, M. A., Horan, K. L., Doody, D. R., Meschke, J. S., Park, D. R., Jackson, L. A., et al. (2012). Environment or host? American Journal of Respiratory and Critical Care Medicine, 186(7), 684–691.

    Article  Google Scholar 

  • Epson, E., & Winthrop, K. (2012). Nontuberculous mycobacterial lung disease: an emerging disease in the elderly. Open Longevity Science, 6, 92–100.

    Article  Google Scholar 

  • Falkinham, J. O., III. (2009). Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. Journal of Applied Microbiology, 107, 356–367.

    Article  CAS  Google Scholar 

  • Falkinham, J. O., III. (2011). Nontuberculous mycobacteria from household plumbing of patients with nontuberculous mycobacteria disease emerging infectious diseases. Research, 17(3), 419–424.

    Google Scholar 

  • Gerogianni, I., Papala, M., Kostikas, K., Petinaki, E., & Gourgoulianis, K. I. (2008). Epidemiology and clinical significance of mycobacterial respiratory infections in central Greece. The International Journal of Tuberculosis and Lung Disease, 12(7), 807–812.

    CAS  Google Scholar 

  • Gill, C. O., Saucier, L., & Meadus, W. J. (2011). Mycobacterium avium subsp. paratuberculosis in dairy products, meat, and drinking water. Journal of Food Protection, 74(3), 480–499.

    Article  CAS  Google Scholar 

  • Gitti, Z., Mantarakis, E., Maraki, S., & Samonis, G. (2011). Clinical significance and antibiotic susceptibilities of nontuberculous mycobacteria from patients in Crete, Greece. Future Microbiology, 6(9), 1099–1109.

    Article  CAS  Google Scholar 

  • Griffith, D. E., Aksamit, T., Brown–Elliott, B. A., Catanzaro, A., Daley, C., Gordin, F., et al. (2007). An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. American Journal of Respiratory and Critical Care Medicine, 175, 367–416.

    Article  CAS  Google Scholar 

  • Hilborn, E. D., Covert, T. C., Yakrus, M. A., Harris, S. I., Donnely, S. F., Rice, E. W., et al. (2006). Persistence of nontuberculous mycobacteria in a drinking water system after addition of filtration treatment. Applied and Environmental Microbiology, 72(9), 5864–5869.

    Article  CAS  Google Scholar 

  • Iseman, M. D., & Marras, T. K. (2008). The importance of nontuberculous mycobacterial lung disease. American Journal of Respiratory and Critical Care Medicine, 178, 999–1001.

    Article  CAS  Google Scholar 

  • Jolobe, O. M. P. (2011). Atypical tuberculous pleural effusions. European Journal of Internal Medicine, 22, 456–459.

    Article  Google Scholar 

  • Kaevska, M., & Hruska, K. (2010). Research on Mycobacterium avium during the period 1995 to 2009. Veterinari Medicina, 55(10), 473–482.

    Google Scholar 

  • Kamala, T., Paramasivan, C. N., Herbert, D., Venkatesan, P., & Prabhakar, R. (1994). Evaluation of procedures for isolation of nontuberculous mycobacteria from soil and water. Applied and Environmental Microbiology, 60(3), 1021–1024.

    CAS  Google Scholar 

  • Kankya, C., Muwonge, A., Djønne, B., Munyeme, M., Opuda-Asibo, J., Skjerve, E., Oloya, J., Edvardsen, V., & Johansen, T. B. (2011). Isolation of non-tuberculous mycobacteria from pastoral ecosystems of Uganda: public health significance. BMC Public Health, 11, 320.

    Article  Google Scholar 

  • Liu, C. W., Lin, K. H., & Kuo, Y. M. (2003). Application of factor analysis in the assessment of groundwater quality in a blackfoot disease area in Taiwan. Science of the Total Environment, 313, 77–89.

    Article  CAS  Google Scholar 

  • Lyu, J., Jang, H. J., Song, J. W., Choi, C. M., Oh, Y. M., Lee, S. D., Kim, W. S., Kim, D. S., & Shim, T. S. (2011). Outcomes in patients with Mycobacterium abscessus pulmonary disease treated with long-term injectable drugs. Respiratory Medicine, 105, 781–787.

    Article  Google Scholar 

  • Maekawa, K., Ito, Y., Hirai, T., Kubo, T., Imai, S., Tatsumi, S., Fujita, K., Takakura, S., Niimi, A., Iinuma, Y., Ichiyama, S., Togashi, K., & Mishima, M. (2011). Environmental risk factors for pulmonary Mycobacterium avium-intracellulare complex disease. CHEST, 140(3), 723–729.

    Article  Google Scholar 

  • Massart, D. L., & Kaufman, L. (1983). The interpretation of chemical data by the use of cluster analysis. New York: Wiley.

    Google Scholar 

  • Mendes dé Souza, M. G., Sato, D. N., Leite, C. Q., de Andrade Leite, S. R., Sartori, F. G., de Andrade Prince, K., Casmeiro, L. A., & Martins, C. H. G. (2010). Occurrence of pathogenic environmental mycobacteria on surfaces in health institutions. Research and Reports in Tropical Medicine, 1, 53–58.

    Google Scholar 

  • Mendoza, J. L., Lana, R., & Diaz-Rubio, M. (2009). Mycobacterium avium subspecies paratuberculosis and its relationship with Crohn’s disease. World Journal of Gastroenterology, 15(4), 417–422.

    Article  CAS  Google Scholar 

  • Moore, J. E., Kruijshaar, M. E., Ormerod, L., Drobniewski, F., & Abubakar, I. (2010). Increasing reports of non-tuberculous mycobacteria in England, Wales and Northern Ireland, 1995–2006. BMC Public Health, 10, 612.

    Article  Google Scholar 

  • Moorthy, R. S., Valluri, S., & Rao, N. A. (2012). Nontuberculous mycobacterial ocular and adnexal infections. Survey of Ophthalmology, 57(3), 202–235.

    Article  Google Scholar 

  • Ness, R., Kip, K., Hillier, S., Soper, D., Stamm, C., Sweet, R., Rice, P., & Richter, H. (2005). A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. American Journal of Epidemiology, 162, 585–590.

    Article  Google Scholar 

  • Neumann, M., Schulze-Robbecke, R., Hagenau, C., & Behringer, K. (1997). Comparison of methods for isolation of mycobacteria from water. Applied and Environmental Microbiology, 63(2), 547–552.

    CAS  Google Scholar 

  • Nguyen, H., Altinger, J., Carrieri-Kohlman, V., Gormley, J., Paul, S., & Stulbarg, M. (2003). Factor analysis of laboratory and clinical measurements of dyspnea in patients with chronic obstructive pulmonary disease. Journal of Pain and Symptom Management, 25, 118–127.

    Article  Google Scholar 

  • Panagiotou, M., Papaioannou, A. I., Kostikas, K., Paraskeua, M., Velentza, E., Kanellopoulou, M., Filaditaki, V., & Karagiannidis, N. (2014). The epidemiology of pulmonary nontuberculous mycobacteria: data from a general hospital in Athens, Greece, 2007–2013. Pulmonary Medicine, 2014, 894976. doi:10.1155/2014/894976.

    Article  Google Scholar 

  • Papaioannou, A., Karamanis, G., Rigas, I., Spanos, T., & Roupa, Z. (2009). Determination and modelling clinical laboratory data of healthy individuals and end-stage renal failure patients. Central European Journal of Medicine, 4(1), 37–48.

    Google Scholar 

  • Papaioannou, A., Mavridou, A., Hadjichristodoulou, C., Papastergiou, P., Pappa, O., Dovriki, E., & Rigas, I. (2010). Application of multivariate statistical methods for groundwater physicochemical and biological quality assessment in the context of public health. Environmental Monitoring and Assessment, 170, 87–97.

    Article  CAS  Google Scholar 

  • Pavlik, I., Matlova, L., Gilar, M., Bartl, J., Parmova, I., Lysak, F., et al. (2007). Isolation of conditionally pathogenic mycobacteria from the environment of one pig farm and the effectiveness of preventive measures between 1997 and 2003. Veterinární Medicína, 52(9), 392–404.

    CAS  Google Scholar 

  • Penn, R., Steehler, M. K., Sokohl, A., & Harley, E. H. (2011). Nontuberculous mycobacterial cervicofacial lymphadenitis—a review and proposed classification system. International Journal of Pediatric Otorhinolaryngology, 75, 1599–1603.

    Article  Google Scholar 

  • Poupard, J., Gagnon, B., Stanhope, M., & Stewart, C. (2002). Methods for data mining from large multinational surveillance studies. Antimicrobial Agents and Chemotherapy, 46, 2409–2419.

    Article  CAS  Google Scholar 

  • Primm, T. P., Lucero, C. A., & Falkinham, J. O., III. (2004). Health impacts of environment mycobacteria. Clinical Microbiology Reviews, 17(1), 98–106.

    Article  Google Scholar 

  • Radomski, N., Cambau, E., Moulin, L., Haenn, S., Moilleron, R., & Lucas, F. S. (2010). Comparison of culture methods for isolation of nontuberculous mycobacteria from surface waters. Applied and Environmental Microbiology, 76(11), 3514–3520.

    Article  CAS  Google Scholar 

  • Rosenblueth, M., Martinez-Romero, J. C., Reyes-Prieto, M., Rogel, M. A., & Martinez-Romero, E. (2011). Environmental mycobacteria: a threat to human health? DNA and Cell Biology, 30(9), 633–640.

    Article  CAS  Google Scholar 

  • Roux, A. L., Catherinot, E., Ripoll, F., Soismier, N., Macheras, E., Ravilly, S., et al. (2009). Multicenter study of prevalence of nontuberculous mycobacteria in patients with cystic fibrosis in France. Journal of Clinical Microbiology, 47(12), 4124–4128.

    Article  Google Scholar 

  • Russell, C. D., Claxton, P., Doig, C., Seagar, A. L., Rayner, A., & Laurenson, I. F. (2014). Non-tuberculous mycobacteria: a retrospective review of Scottish isolates from 2000 to 2010. Thorax, 69, 593–595.

    Article  Google Scholar 

  • Schultze-Robbecke, R., Weber, A., & Fischeder, R. J. (1991). Microbiological methods, 14, 177.

    Article  Google Scholar 

  • Singh, K. P., Malik, A., & Sinha, S. (2005). Water quality assessment and apportionment of pollution sources of Gomti river (India) using multivariate statistical techniques: a case study. Analytica Chimica Acta, 538, 355–374.

    Article  CAS  Google Scholar 

  • Thomson, R. M., Carter, R., Tolson, C., Coulter, C., Huygens, F., & Hargreaves, M. (2013). Factors associated with the isolation of nontuberculous mycobacteria (NTM) from a large municipal water system in Brisbane, Australia. BMC Microbiology, 13, 89.

    Article  Google Scholar 

  • Tichenor, W. S., Thurlow, J., McNulty, S., Brown-Elliott, B. A., Wallace, R. J., & Falkinham, J. O., III. (2012). Nontuberculous mycobacteria in household plumbing as possible cause of chronic rhinosinusitis. Emerging Infectious Diseases, 18(10), 1612–1617.

    Article  CAS  Google Scholar 

  • Torvinen, E., Suomalainen, S., Lehtola, M. J., Miettinen, I. T., Zacheus, O., Paulin, L., et al. (2004). Mycobacteria in water and loose deposits of drinking water distribution systems in Finland. Applied and Environmental Microbiology, 70(4), 1973–1981.

    Article  CAS  Google Scholar 

  • Tsintzou, A., Vantarakis, A., Pagonopoulou, O., Athanassiadou, A., & Papapetropoulou, M. (2000). Environmental mycobacteria in drinking water before and after replacement of the water distribution network. Water, Air, and Soil Pollution, 120, 273–282.

    Article  CAS  Google Scholar 

  • Vanderginste, B., Massart, D. L., Buydens, L., De Jong, S., Lewi, P., & Smeyers-Verbeke, J. (1998). Handbook of chemometrics and qualimetrics. Amsterdam: Elsevier.

    Google Scholar 

  • Vantarakis, A., Tsintzou, A., Diamandopoulos, A., & Papapetropoulou, M. (1998). Non-tuberculous mycobacteria in hospital water supplies. Water, Air, and Soil Pollution, 104, 331–337.

    Article  CAS  Google Scholar 

  • Vogt, W., & Nagel, D. (1992). Cluster analysis in diagnosis. Clinical Chemistry, 38, 182–198.

    CAS  Google Scholar 

  • Whiley, H., Keegan, A., Giglio, S., & Bentham, R. (2012). Mycobacterium avium complex—the role of potable water in disease transmission. Journal of Applied Microbiology, 113, 223–232.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Respiratory Medicine, Medical School, University of Thessaly, Larissa, Greece

    Eleni Dovriki, Irini Gerogianni & Kostas Gourgoulianis

  2. Department of Microbiology, Medical School, University of Larissa, Larissa, Greece

    Efi Petinaki

  3. Department of Hygiene and Epidemiology, School of Medicine, University of Thessaly, Larissa, Greece

    Christos Hadjichristodoulou

  4. Department of Medical Laboratories, Technological Education Institution of Thessaly, Larissa, Greece

    Agelos Papaioannou

Authors
  1. Eleni Dovriki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irini Gerogianni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Efi Petinaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christos Hadjichristodoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agelos Papaioannou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kostas Gourgoulianis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eleni Dovriki.

Ethics declarations

The study was approved by the Ethics Committee of the University of Thessaly. All patients were informed and provided their written consent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dovriki, E., Gerogianni, I., Petinaki, E. et al. Isolation and identification of nontuberculous mycobacteria from hospitalized patients and drinking water samples—examination of their correlation by chemometrics. Environ Monit Assess 188, 247 (2016). https://doi.org/10.1007/s10661-016-5258-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-016-5258-7

Keywords

Search

Navigation