Printer Friendly

A Review of Nontuberculous Mycobacteria Presence in Raw and Pasteurized Bovine Milk.

Introduction

Nontuberculous mycobacteria (NTM) include all Mycobacterium species excluding M. tuberculosis complex and can also be referred to as environmental mycobacteria (Falkinham, 1996). Presently there are more than 120 recognized species of NTM and of those, 42 have been identified as opportunistic human pathogens of public health significance (Myneedu et al., 2013). NTM are ubiquitous in the environment and have been found in salt water, hard water, hot water systems, soils, dust, food, and plants (Ministry of Health, 2002). Humanto-human transmission of NTM is rare, so it is important to understand the environmental sources associated with human infection (Kankya et al., 2011).

Historically, the presence of Mycobacterium spp. in milk, specifically M. bovis, has received a lot of attention as a potential source of tuberculosis (Davies, 2006). In developed countries this route of exposure is now rare due to milk pasteurization processes and culling of infected herds (Centers for Disease Control and Prevention, 2005). This route of exposure is still an issue in developing countries and when raw milk is consumed (Muller et al., 2013). In developed countries, Mycobacterium spp. are once again receiving a lot of attention, however, because NTM are the focus of an increasing incidence of diseases caused by opportunistic pathogens (Mirsaeidi, Farshidpour, Allen, Ebrahimi, & Falkinham, 2014).

Increases in the incidence of NTM infections have been observed all around the world (Kendall & Winthrop, 2013; Panagiotou et al., 2014; Yoo et al., 2012). In Taiwan, from the years 2000-2008, the incidence of NTM disease increased from 2.7 to 10.2 cases per 100,000 (Lai et al., 2010) and in England, Wales, and Northern Ireland, the incidence of NTM infection increased from 0.9 per 100,000 population in 1995 to 2.9 per 100,000 in 2006 (Moore, Kruijshaar, Ormerod, Drobniewski, & Abubakar, 2010). The increase in incidence in NTM infection highlights the need to understand more about potential sources of infection. This review will explore the possible role of bovine milk as a potential source of NTM.

Methods

Original research articles investigating the presence of NTM in bovine milk samples published in English over the last 20 years were searched using Google scholar and Scopus (Table 1). The country the milk was sampled from, the detection method used, and the type of milk is also presented in Table 1. The reliability of different detection methods and the potential for NTM to survive the milk pasteurization process is also discussed.

NTM and Unpasteurized Milk

Worldwide NTM have been detected in raw milk samples as demonstrated by Table 1. The most commonly isolated species are Mycobacterium avium complex (MAC) and specifically M. avium subspecies paratuberculosis (MAP), which has been detected using culture in raw milk samples from Cyprus, the Czech Republic, Denmark, India, Ireland, Italy, Tanzania, UK, and U.S. (Ayele, Svastova, Roubal, Bartos, & Pavlik, 2005; Botsaris et al., 2010; Grant, Ball, & Rowe, 2002; Mdegela et al., 2005; O'Reilly et al., 2004; Pillai & Jayarao, 2002; Shankar et al., 2010; Slana, Kralik, Kralova, & Pavlik, 2008; Taddei et al., 2008). MAP has also been detected using PCR in raw milk from Austria, Chile, Cyprus, the Czech Republic, Denmark, India, Ireland, Switzerland, and UK (Ayele et al., 2005; Botsaris et al., 2010; Corti & Stephan, 2002; Giese & Ahrens, 2000; Khol et al., 2013; Kruze, Monti, Schulze, Mella, & Leiva, 2013; O'Reilly et al., 2004; Shankar et al., 2010; Slana, Liapi, Moravkova, Kralova, & Pavlik, 2009).

Other NTM that have been detected in raw milk samples, as shown in Table 1, include M. nonchromogenicum, M. peregrinum, M. smegmatis, M. neoaurum, M. fortuitum, M. kansasii, M. scrofulaceum, M. gordonae, M. flavescens, M. duvalii, M. haemophilum, M. immunogenum, M. lentiflavum, M. mucogenicum, M. novocastrense, M. parafortuitum, M. terrae, M. vaccae, M. simiae, M. porcinum, M. agri, M. phlei, and M. marinum (Franco et al., 2013; Fujimura Leite et al., 2003; Jordao Junior, Lopes, David, Farache Filho, & Leite, 2009; Kazwala et al., 1998; Konuk, Korcan, Dulgerbaki, & Altindis], 2007; Mdegela et al., 2005; Sgarioni et al., 2014; Slana et al., 2009; Taddei et al., 2008).

The presence of NTM in raw milk could be attributed to bovine hosts (Animal Health Australia, 2017; Diguimbaye-Djaibe et al., 2006; Pavlik, Matlova, Dvorska, Shitaye, & Parmova, 2005) or through cross-contamination with environmental sources (Eltholth, Marsh, Van Winden, & Guitian, 2009), or both. In South Africa it has been demonstrated that NTM are readily exchanged back and forth between water/soil and cattle/water buffalo through the mucous membranes of the animals (Gcebe, Rutten, Gey van Pittius, & Michel, 2013).

NTM and Pasteurized Milk

MAP has been the focus of the majority of research into the presence of NTM in pasteurized milk as shown in Table 1. MAP has been detected, using culture methods, in commercially available pasteurized milk from Brazil (Carvalho, Pietralonga, Schwarz, Faria, & Moreira, 2012), India, the Czech Republic, U.S., Argentina, and the UK (Ayele et al., 2005; Carvalho et al., 2012; Ellingson et al., 2005; Grant et al., 2002; Paolicchii et al., 2003; Shankar et al., 2010) and has also been detected using PCR in pasteurized milk from India, Iran, Ireland, and the UK (Anzabi & Hanifian, 2012; Grant et al., 2002; Millar et al., 1996; O'Reilly et al., 2004; Shankar et al., 2010). Other NTM that have been detected in pasteurized milk using culture include M. chelonae, M. peregrinum, M. fortuitum, M. marinum, M. kansasii and M. gordonae (Fujimura Leite et al., 2003; Sgarioni et al., 2014). The presence of NTM in pasteurized milk could be due to cross-contamination after the pasteurization processes or survival of the pasteurization process (Eisenberg et al., 2010; Van Brandt et al., 2011). Despite the presence of NTM in pasteurized milk samples from across the globe, there are currently no reported case studies of NTM infection that identify milk as a definitive source of infection.

NTM Potential to Survive Milk Pasteurization

The potential for NTM to survive the milk pasteurization process is supported by several experimental studies that have been focused specifically on the survival of MAP (Grant, Ball, & Rowe, 1998; Meylan et al., 1996; Peterz, Butot, Jagadeesan, Bakker, & Donaghy, 2016; Starikoff, Nishimoto, Ferreira, Balian, & Telles, 2016; Van Brandt et al., 2011). The effectiveness of the pasteurization process has been shown to be dependent on a range of variables, including pressure, time, and temperature (Grant, Williams, Rowe, & Muir, 2005). Donaghy and coauthors (2007) investigated the effect of pressure and time on the survival of MAP. It was found that pasteurization at 500 MPa resulted in a significantly (p < .05) greater reduction of MAP compared to 400 MPa. It was also demonstrated that a treatment time of 10 min significantly (p < .05) reduced MAP numbers compared with a treatment time of 5 min.

There are also conflicting observations from studies investigating the potential heat resistance of MAP (Lund, Gould, & Rampling, 2002; Rademaker, Vissers, & Te Giffel, 2007). Stabel and coauthors (1997) demonstrated that in a laboratory experiment MAP (at concentrations of [10.sup.4] and [10.sup.6] CFU/mL) was inactivated by heat treatment at temperatures of 72 [degrees]C and greater for at least 15 s. This finding was supported by Rademaker and coauthors (2007) who demonstrated that heat treatment at 72 [degrees]C for 15 s resulted in a greater than 7-fold reduction of MAP. These results differ, however, from other studies that demonstrated the survival of MAP at 72 [degrees]C for 15 s (Grant et al., 1998; Sung & Collins, 1998). Additionally, Van Brandt and coauthors (2011) demonstrated that in two out of six replicate experiments the HTST pasteurization conditions (71.7 [degrees]C, 15 s) were not sufficient to inactivate MAP in milk. It has been suggested that the discrepancy in these results might be due to the tendency of MAP cells to clump together and a possibility that there is a protective effect of certain milk components on MAP (Lindstrom, Paulsson, Nylander, Elofsson, & Linkmark-Mansson, 1994). This tendency could contribute to its heat resistance and potential survival of commercial milk pasteurization processes (Klijn, Herrewegh, & de Jong, 2001; Rowe, Grant, Dundee, & Ball, 2000). Research by Peterz and coauthors (2016) has demonstrated the efficiency of direct stream injection for inactivating MAP, which presents an alternative novel method to optimise the pasteurization process. The complete elimination of MAP by pasteurization, however, is still under debate.

NTM Detection Methods

Currently there is no standard method for NTM detection, although as demonstrated by Table 1, the main methods used are culture and PCR. The main variations in NTM culture methodology relate to the decontamination step and the culture medium used. A decontaminated process is not always included (Giese & Ahrens, 2000; Paolicchii et al., 2003); however, when it is, the most common method uses 0.75% hexadecylpyridinium chloride (HPC). This method has been successfully used when detecting NTM from cheese as well as raw and pasteurized milk (Anzabi & Hanifian, 2012; Botsaris et al., 2010; Carvalho et al., 2012; Faria et al., 2014; O'Reilly et al., 2004; Taddei et al., 2008). Other decontamination methods include using 5% oxalic acid, which has been used for the detection of NTM in raw and pasteurized milk (Fujimura Leite et al., 2003; Sgarioni et al., 2014). Also the Petroff's decontamination method has been used to detect NTM in raw buffalo milk (Jordao Junior et al., 2009); using SDS-NaOH (Konuk et al., 2007), or 4% sodium hydroxide neutralized with 14% potassium dihydrogen orthophosphate (Mdegela et al., 2005) has been used to detect NTM from raw cow's milk.

The most common media used is the Herrold's egg yolk medium (HEYM) (Anzabi & Hanifian, 2012; Botsaris et al., 2010; Carvalho et al., 2012; Faria et al., 2014; Grant et al., 2002; Pillai & Jayarao, 2002), although additions or alterations to this medium are also reported. Anzabi and Hanifian (2012) used HEYM with and without 2 [micro]L/mL of mycobactin J and amphotericin B, nalidixic acid, and vancomycin for culture. Taddei and coauthors (2008) used HEYM containing 2 [micro]g of mycobactin J/mL supplemented with chloramphenical (30 [micro]g/L) or nalidixic acid (50 [micro]g/L) and vancomycin (50 [micro]g/L). Ayele and coauthors (2005) cultured milk on HEYM slants.

Ellingson and coauthors (2005) cultured milk on HEYM slants with mycobactin J and amphotericin B, nalidixic acid, and vancomycin. O'Reilly and coauthors (2004) cultured milk on HEYM containing 2 g of mycobactin J/mL and BACTEC 12B radiometric medium supplemented with 0.5 mL of Difco egg yolk emulsion, 2 g of mycobactin J/mL, and PANTA antibiotic supplement. Other culture mediums included Lowenstein Jensen media (Franco et al., 2013; Konuk et al., 2007), Lowenstein-Jensen medium with added pyruvate (Kazwala et al., 1998), and Lowenstein-Jensen and Stonebrink's media (Fujimura Leite et al., 2003; Jordao Junior et al., 2009; Sgarioni et al., 2014). The lack of standardization regarding culture medium makes it challenging to compare results from different studies. It also identifies that there is a lack of consensus regarding the best medium for NTM isolation.

There are numerous studies that compare different NTM detection methods (Damato & Collins, 1990; Kamala, Paramasivan, Herbert, Venkatesan, & Prabhakar, 1994; Thomson, Carter, Gilpin, Coulter, & Hargreaves, 2008). There are limited studies, however, that look specifically at NTM detection in milk and the studies that do focus on MAP. Dundee and coauthors (2001) compared four decontamination methods for the culture of MAP from milk and found pretreatment with 0.75% HPC for 5 hr to be the most efficient method, yielding the higher percentage recovery of MAP with the lowest limit of detection. Grant and coauthors (2003) compared nonradiometric mycobacteria growth indicator tubes and radiometric BACTEC 460TB culture systems as methods to identify MAP from milk and found there to be little difference between the two methods.

The biggest difficulty with the culture method of detection is that it is time consuming because of the organism's fastidious nature and slow growth (Mendoza, Lana, & Diaz-Rubio, 2009). Also, further identification methods are required to determine the specific Mycobacterium species (Franco et al., 2013). The main alternative method to culture detection is PCR (Table 1). Once again, MAP detection has received the most attention and multiple gene targets for MAP PCR have been identified including IS900, F57, ISMav2, hspX, and ISMap02 (Ellingson, Bolin, & Stabel, 1998; Mobius, Hotzel, Rassbach, & Kohler, 2008; Stabel & Bannantine, 2005). The most commonly used is IS900, which is found only in MAP genome; however, there have been reports of cross-reactions with other Mycobacterium species (Cousins et al., 1999). The main disadvantage with PCR is that it does not differentiate between viable organism and killed cells (Ricchi et al., 2014).

Conclusion

With aging populations, opportunistic pathogens are becoming a significant issue of public health concern. As the incidence of NTM infections increases, there is a greater need to identify the sources of infection. The presence of NTM in milk and the potential of NTM to survive the pasteurization process might present a possible risk to public health. This review demonstrates that NTM have been detected in raw and pasteurized milk sampled across the globe. Comparing these studies and factors influencing the presence of NTM, however, is difficult due to a number of variables. This difficulty includes the potential for herds to be infected with MAP, variances in sampling and detection methodologies, reliability and reproducibility of detection methods, and differences in the pasteurization operational procedures. In addition, although NTM are present in milk, there currently is no clinical evidence demonstrating that milk is a route of exposure; further research is required to determine the potential role milk might be playing as a source of NTM disease. If milk is identified as a source of infection, there is also a need for the development of appropriate management and control measures. Included in these measures will be ensuring the success of pasteurization methods for the elimination on NTM.

Corresponding Author: Harriet Whiley, Environmental Health, College of Science and Engineering, Flinders University, GPO Box 2100, Adelaide, 5001, Australia.

E-mail: harriet.whiley@flinders.edu.au.

References

Anzabi, Y., & Hanifian, S. (2012). Detection of Mycobacterium avium subspecies paratuberculosis in pasteurized milk by IS900 PCR and culture method. African Journal of Microbiology Research, 6(7), 1453-1456.

Animal Health Australia. (2017). Johne's disease in cattle. Retrieved from https://www.animalhealthaustralia.com.au/what-we-do/ endemic-disease/johnes-disease-in-cattle

Ayele, W.Y., Svastova, P, Roubal, P, Bartos, M., & Pavlik, I. (2005). Mycobacterium avium subspecies paratuberculosis cultured from locally and commercially pasteurized cow's milk in the Czech Republic. Applied and Environmental Microbiology, 71(3), 1210-1214.

Bezerra, A.V., Dos Reis, E.M., Rodrigues, R.O., Cenci, A., Cerva, C., & Mayer, F.Q. (2015). Detection of Mycobacterium tuberculosis and Mycobacterium avium complexes by real-time PCR in bovine milk from Brazilian dairy farms. Journal of Food Protection, 78(5), 1037-1042.

Botsaris, G., Slana, I., Liapi, M., Dodd, C., Economides, C., Rees, C., & Pavlik, I. (2010). Rapid detection methods for viable Mycobacterium avium subspecies paratuberculosis in milk and cheese. International Journal of Food Microbiology, 141 (Suppl. 1), S87-90.

Carvalho, I.A., Pietralonga, PA., Schwarz, D.G., Faria, A.C., & Moreira, M.A. (2012). Short communication: Recovery of viable Mycobacterium avium subspecies paratuberculosis from retail pasteurized whole milk in Brazil. Journal of Dairy Science, 95(12), 6946-6948.

Centers for Disease Control and Prevention. (2005). Human tuberculosis caused by Mycobacterium bovis--New York City, 20012004. Morbidity and Mortality Weekly Report, 54(24), 605-608.

Corti, S., & Stephan, R. (2002). Detection of Mycobacterium avium subspecies paratuberculosis specific IS900 insertion sequences in bulk-tank milk samples obtained from different regions throughout Switzerland. BMC Microbiology, 2(1), 15.

Cousins, D.V, Whittington, R., Marsh, I., Masters, A., Evans, R.J., & Kluver, P (1999). Mycobacteria distinct from Mycobacterium avium subsp. paratuberculosis isolated from the faeces of ruminants possess IS900-like sequences detectable by IS900 polymerase chain reaction: Implications for diagnosis. Molecular and Cellular Probes, 13(6), 431-442.

Damato, J.J., & Collins, M.T. (1990). Growth of Mycobacterium paratuberculosis in radiometric, Middlebrook and egg-based media. Veterinary Microbiology, 22(1), 31-42.

Davies, P.D.O. (2006). Tuberculosis in humans and animals: Are we a threat to each other? Journal of the Royal Society of Medicine, 99(10), 539-540.

Diguimbaye-Djaibe, C., Vincent, V, Schelling, E., Hilty, M., Ngandolo, R., Mahamat, H.H., ... Zinsstag, J. (2006). Species identification of non-tuberculous mycobacteria from humans and cattle of Chad. Schweizer Archiv fur Tierheilkunde, 148(5), 251-256.

Donaghy, J.A., Linton, M., Patterson, M.F, & Rowe, M.T. (2007). Effect of high pressure and pasteurization on Mycobacterium avium ssp. paratuberculosis in milk. Letters in Applied Microbiology, 45(2), 154-159.

Dundee, L., Grant, I.R., Ball, H.J., & Rowe, M.T. (2001). Comparative evaluation of four decontamination protocols for the isolation of Mycobacterium avium subsp. paratuberculosis from milk. Letters in Applied Microbiology, 33(3), 173-177.

Eisenberg, S.W.E, Koets, A.P, Hoeboer, J., Bouman, M., Heederik, D., & Nielen, M. (2010). Presence of Mycobacterium avium subsp. paratuberculosis in environmental samples collected on commercial Dutch dairy farms. Applied and Environmental Microbiology, 76(18), 6310-6312.

Ellingson, J.L., Anderson, J.L., Koziczkowski, J.J., Radcliff, R.P, Sloan, S.J., Allen, S.E., & Sullivan, N.M. (2005). Detection of viable Mycobacterium avium subsp. paratuberculosis in retail pasteurized whole milk by two culture methods and PCR. Journal of Food Protection, 68(5), 966-972.

Ellingson, J.L., Bolin, C.A., & Stabel, J.R. (1998). Identification of a gene unique to Mycobacterium avium subspecies paratuberculosis and application to diagnosis of paratuberculosis. Molecular and Cellular Probes, 12(3), 133-142.

Eltholth, M.M., Marsh, V.R., Van Winden, S., & Guitian, EJ. (2009). Contamination of food products with Mycobacterium avium paratuberculosis: A systematic review. Journal of Applied Microbiology, 107(4), 1061-1071.

Ealkinham, J.O., III. (1996). Epidemiology of infection by nontuberculous mycobacteria. Clinical Microbiology Reviews, 9(2), 177-215.

Earia, A.C., Schwarz, D.G., Carvalho, I.A., Rocha, B.B., De Carvalho Castro, K.N., Silva, M.R., & Moreira, M.A. (2014). Short communication: Viable Mycobacterium avium subspecies paratuberculosis in retail artisanal Coalho cheese from Northeastern Brazil. Journal of Dairy Science, 97(7), 4111-4114.

Eathi, R., Sarkarati, E, Eslami, M., Rezavand, B., & Nourizadeh, A. (2011). Detection of Mycobacterium avium subsp. paratuberculosis in cow milk using culture and PCR methods. Archives of Razi Institute, 66(2).

Franco, M.M., Paes, A.C., Ribeiro, M.G., de Eigueiredo Pantoja, J.C., Santos, A.C., Miyata, M., ... Listoni, EJ. (2013). Occurrence of mycobacteria in bovine milk samples from both individual and collective bulk tanks at farms and informal markets in the southeast region of Sao Paulo, Brazil. BMC Veterinary Research, 9(1), 85.

Eujimura Leite, C.Q., Anno, I.S., de Andrade Leite, S.R., Roxo, E., Morlock, G.P, & Cooksey, R.C. (2003). Isolation and identification of mycobacteria from livestock specimens and milk obtained in Brazil. Memorias do Instituto Oswaldo Cruz, 98(3), 319-323.

Gcebe, N., Rutten, V, Gey van Pittius, N.C., & Michel, A. (2013). Prevalence and distribution of non-tuberculous mycobacteria (NTM) in cattle, African buffaloes (Syncerus caffer), and their environments in South Africa. Transboundary and Emerging Diseases, 60(Suppl. 1), 74-84.

Giese, S.B., & Ahrens, P (2000). Detection of Mycobacterium avium subsp. paratuberculosis in milk from clinically affected cows by PCR and culture. Veterinary Microbiology, 77(3-4), 291-297.

Grant, I.R., Ball, H.J., & Rowe, M.T. (1998). Effect of high-temperature, short-time (HTST) pasteurization on milk containing low numbers of Mycobacterium paratuberculosis. Letters in Applied Microbiology, 26(2), 166-170.

Grant, I.R., Ball, H.J., & Rowe, M.T. (2002). Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows' milk from approved dairy processing establishments in the United Kingdom. Applied and Environmental Microbiology, 68(5), 2428-2435.

Grant, I.R., Kirk, R.B., Hitchings, E., & Rowe, M.T. (2003). Comparative evaluation of the MGIT and BACTEC culture systems for the recovery of Mycobacterium avium subsp. paratuberculosis from milk. Journal of Applied Microbiology, 95(1), 196-201.

Grant, I.R., Williams, A.G., Rowe, M.T., & Muir, D.D. (2005). Efficacy of various pasteurization time-temperature conditions in combination with homogenization on inactivation of Mycobacterium avium subsp. paratuberculosis in milk. Applied and Environmental Microbiology, 71(6), 2853-2861.

Hanifian, S., & Khani, S. (2016). Tracking of Mycobacterium avium Paratuberculosis load in milk production chain: A real-time qPCR and culture assay. Journal of Food Safety, 36(1), 136-141.

Hassan, K.I., & Ali, A.A. (2012). Detection of Mycobacterium avium in milk powder using species specific PCR. International Journal of Advanced Science and Engineering Technology On Line, 2(2), 115-119.

Hruska, K., Bartos, M., Kralik, P, & Pavlik, I. (2005). Mycobacterium avium subsp. paratuberculosis in powdered infant milk: Paratuberculosis in cattle--The public health problem to be solved. Veterinarnl Medicina, 50(8), 327-335.

Hruska, K., Slana, I., Kralik, P, & Pavlik, I. (2011). Mycobacterium avium subsp. paratuberculosis in powdered infant milk: E57 competitive real time PCR. Veterindrni Medicina, 56(5), 226-230.

Jordao Junior, C.M., Lopes, EC., David, S., Earache Eilho, A., & Leite, C.Q. (2009). Detection of nontuberculous mycobacteria from water buffalo raw milk in Brazil. Food Microbiology, 26(6), 658-661.

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.

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

Kazwala, R.R., Daborn, C.J., Kusiluka, L.J., Jiwa, S.E, Sharp, J.M., & Kambarage, D.M. (1998). Isolation of Mycobacterium species from raw milk of pastoral cattle of the Southern Highlands of Tanzania. Tropical Animal Health and Production, 30(4), 233-239.

Kendall, B.A., & Winthrop, K.L. (2013). Update on the epidemiology of pulmonary nontuberculous mycobacterial infections. Seminars in Respiratory and Critical Care Medicine, 34(1), 87-94.

Khol, J.L., Wassertheurer, M., Sodoma, E., Revilla-Fernandez, S., Damoser, J., Osterreicher, E., ... Baumgartner, W. (2013). Long-term detection of Mycobacterium avium subspecies paratuberculosis in individual and bulk tank milk from a dairy herd with a low prevalence of Johne's disease. Journal of Dairy Science, 96(6), 3517-3524.

Klijn, N., Herrewegh, A., & de Jong, P. (2001). Heat inactivation data for Mycobacterium avium subsp. paratuberculosis: Implications for interpretation. Journal of Applied Microbiology, 91(4), 697-704.

Konuk, M., Korcan, E., Dulgerbaki, S., & Altindis, M. (2007). Isolation and identification of mycobacteria from raw milk samples in Afyonkarahisar district of Turkey. International Journal of Food Microbiology, 115(3), 343-347.

Kruze, J., Monti, G., Schulze, F, Mella, A., & Leiva, S. (2013). Herd-level prevalence of Map infection in dairy herds of southern Chile determined by culture of environmental fecal samples and bulk-tank milk qPCR. Preventive Veterinary Medicine, 111(3-4), 319-324.

Lai, C.C., Tan, C.K., Chou, C.H., Hsu, H.L., Liao, C.H., Huang, Y.T., ... Hsueh, PR. (2010). Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000-2008. Emerging Infectious Diseases, 16(2), 294-296.

Lindstrom, P, Paulsson, M., Nylander, T., Elofsson, U., & Lindmark-Mansson, H. (1994). The effect of heat treatment on bovine immunoglobulins. Milchwissenschaft, 49(2), 67-71.

Lund, B.M., Gould, G.W., & Rampling, A.M. (2002). Pasteurization of milk and the heat resistance of Mycobacterium avium subsp. paratuberculosis: A critical review of the data. International Journal of Food Microbiology, 77(1-2), 135-145.

Mdegela, R.H., Karimuribo, E., Kusiluka, L.J.M., Kabula, B., Manjurano, A., Kapaga, A.M., & Kambarage, D.M. (2005). Mastitis in smallholder dairy and pastoral cattle herds in the urban and peri-urban areas of the Dodoma municipality in Central Tanzania. Livestock Research for Rural Development, 17(11).

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

Meylan, M., Rings, D.M., Shulaw, W.P, Kowalski, J.J., Bech-Nielsen, S., & Hoffsis, G.F (1996). Survival of Mycobacterium paratuberculosis and preservation of immunoglobulin G in bovine colostrum under experimental conditions simulating pasteurization. American Journal of Veterinary Research, 57(11), 1580-1585.

Millar, D., Ford, J., Sanderson, J., Withey, S., Tizard, M., Doran, T., & Hermon-Taylor, J. (1996). IS900 PCR to detect Mycobacterium paratuberculosis in retail supplies of whole pasteurized cows' milk in England and Wales. Applied and Environmental Microbiology, 62(9), 3446-3452.

Ministry of Health. (2002). Guidelines for tuberculosis control in New Zealand 2003. Wellington, New Zealand: Author. Retrieved from http://www.tbonline.info/media/uploads/documents/guidelines_ for_tuberculosis_control_in_new_zealand_%282003%29.pdf

Mirsaeidi, M., Farshidpour, M., Allen, M.B., Ebrahimi, G., & Falkinham, J.O. (2014). Highlight on advances in nontuberculous mycobacterial disease in North America. BioMed Research International, 2014.

Mobius, P, Hotzel, H., Rassbach, A., & Kohler, H. (2008). Comparison of 13 single-round and nested PCR assays targeting IS900, ISMav2, f57, and locus 255 for detection of Mycobacterium avium subsp. paratuberculosis. Veterinary Microbiology, 126(4), 324-333.

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

Muller, B., Durr, S., Alonso, S., Hattendorf, J., Laisse, C., Parsons, S.D.C., ... Zinsstag, J. (2013). Zoonotic Mycobacterium bovis-induced tuberculosis in humans. Emerging Infectious Diseases, 19(6), 899-908.

Myneedu, VP, Verma, A.K., Bhalla, M., Arora, J., Reza, S., Sah, G.C., & Behera, D. (2013). Occurrence of non-tuberculous mycobacterium in clinical samples--A potential pathogen. Indian Journal of Tuberculosis, 60, 71-76.

O'Reilly, C.E., O'Connor, L., Anderson, W., Harvey, P, Grant, I.R., Donaghy, J., ... O'Mahony, P (2004). Surveillance of bulk raw and commercially pasteurized cows' milk from approved Irish liquid-milk pasteurization plants to determine the incidence of Mycobacterium paratuberculosis. Applied and Environmental Microbiology, 70(9), 5138-5144.

Panagiotou, M., Papaioannou, A.I., Kostikas, K., Paraskeua, M., Velentza, E., Kanellopoulou, M., ... Karagiannidis, N. (2014). The epidemiology of pulmonary nontuberculous mycobacteria: Data from a general hospital in Athens, Greece, 2007-2013. Pulmonary Medicine, 2014.

Paolicchii, FA., Zumarraga, M.J., Gioffre, A., Zamorano, P, Morsella, C., Verna, A., ... Romano, M. (2003). Application of different methods for the diagnosis of paratuberculosis in a dairy cattle herd in Argentina. Journal of Veterinary Medicine, Series B, 50(1), 20-26.

Pavlik, I., Matlova, L., Dvorska, L., Shitaye, J.E., & Parmova, I. (2005). Mycobacterial infections in cattle and pigs caused by Mycobacterium avium complex members and atypical mycobacteria in the Czech Republic during 2000-2004. Veterinarni Medicina, 50(7), 281-290.

Peterz, M., Butot, S., Jagadeesan, B., Bakker, D., & Donaghy, J. (2016). Thermal inactivation of Mycobacterium avium subsp. paratuberculosis in artificially contaminated milk by direct steam injection (DSI). Applied and Environmental Microbiology, 82(9), 2800-2808.

Pillai, S.R., & Jayarao, B.M. (2002). Application of IS900 PCR for detection of Mycobacterium avium subsp. paratuberculosis directly from raw milk. Journal of Dairy Science, 85(5), 1052-1057.

Rademaker, J.L., Vissers, M.M., & Te Giffel, M.C. (2007). Effective heat inactivation of Mycobacterium avium subsp. paratuberculosis in raw milk contaminated with naturally infected feces. Applied and Environmental Microbiology, 73(13), 4185-4190.

Ricchi, M., De Cicco, C., Kralik, P., Babak, V., Boniotti, M.B., Savi, R., ... Arrigoni, N. (2014). Evaluation of viable Mycobacterium avium subsp. paratuberculosis in milk using peptide-mediated separation and Propidium Monoazide qPCR. FEMS Microbiology Letters, 356(1), 127-133.

Rowe, M.T., Grant, I.R., Dundee, L., & Ball, H.J. (2000). Heat resistance of Mycobacterium avium subsp. paratuberculosis in milk. Irish Journal of Agricultural and Food Research, 39(2), 203-208.

Sgarioni, S.A., Hirata, R.D., Hirata, M.H., Leite, C.Q., de Prince, K.A., de Andrade Leite, S.R., ... Cardoso, R.F (2014). Occurrence of Mycobacterium bovis and non-tuberculous mycobacteria (NTM) in raw and pasteurized milk in the northwestern region of Parana, Brazil. Brazilian Journal of Microbiology, 45(2), 707-711.

Shankar, H., Singh, S.V, Singh, P.K., Singh, A.V, Sohal, J.S., & Greenstein, R.J. (2010). Presence, characterization, and genotype profiles of Mycobacterium avium subspecies paratuberculosis from unpasteurized individual and pooled milk, commercial pasteurized milk, and milk products in India by culture, PCR, and PCR-REA methods. International Journal of Infectious Diseases, 14(2), e121-126.

Slana, I., Kralik, P., Kralova, A., & Pavlik, I. (2008). On-farm spread of Mycobacterium avium subsp. paratuberculosis in raw milk studied by IS900 and F57 competitive real time quantitative PCR and culture examination. International Journal of Food Microbiology, 128(2), 250-257.

Slana, I., Liapi, M., Moravkova, M., Kralova, A., & Pavlik, I. (2009). Mycobacterium avium subsp. paratuberculosis in cow bulk tank milk in Cyprus detected by culture and quantitative IS900 and F57 realtime PCR. Preventive Veterinary Medicine, 89(3-4), 223-226.

Stabel, J.R., & Bannantine, J.P (2005). Development of a nested PCR method targeting a unique multicopy element, ISMap02, for detection of Mycobacterium avium subsp. paratuberculosis in fecal samples. Journal of Clinical Microbiology, 43(9), 4744-4750.

Stabel, J.R., Steadham, E.M., & Bolin, C.A. (1997). Heat inactivation of Mycobacterium paratuberculosis in raw milk: Are current pasteurization conditions effective? Applied and Environmental Microbiology, 63(12), 4975-4977.

Starikoff, K.R., Nishimoto, E.J., Ferreira, E, Balian, S.C., & Telles, E.O. (2016). Influence of milk fat in the resistance of Mycobacterium fortuitum to slow pasteurization. Ciencia Animal Brasileira, 17(1), 70-78.

Sung, N., & Collins, M.T. (1998). Thermal tolerance of Mycobacterium paratuberculosis. Applied and Environmental Microbiology, 64(3), 999-1005.

Taddei, R., Barbieri, I., Pacciarini, M.L., Fallacara, E, Belletti, G.L., & Arrigoni, N. (2008). Mycobacterium porcinum strains isolated from bovine bulk milk: Implications for Mycobacterium avium subsp. paratuberculosis detection by PCR and culture. Veterinary Microbiology, 130(3-4), 338-347.

Thomson, R., Carter, R., Gilpin, C., Coulter, C., & Hargreaves, M. (2008). Comparison of methods for processing drinking water samples for the isolation of Mycobacterium avium and Mycobacterium intracellulare. Applied and Environmental Microbiology, 74(10), 3094-3098.

Van Brandt, L., Van der Plancken, I., De Block, J., Vlaemynck, G., Van Coillie, E., Herman, L., & Hendrickx, M. (2011). Adequacy of current pasteurization standards to inactivate Mycobacterium paratuberculosis in milk and phosphate buffer. International Dairy Journal, 21(5), 295-304.

Yoo, J.-W, Jo, K.-W., Kim, M.N., Lee, S.D., Kim, W.S., Kim, D.S., & Shim, T.S. (2012). Increasing trend of isolation of non-tuberculous mycobacteria in a tertiary university hospital in South Korea. Tuberculosis and Respiratory Diseases, 72(5), 409-415.

Harriet Whiley

Shraddha Adhikari

Thilini Piushani Keerthirathne

Tanya Caro Tohme

Environmental Health

College of Science and Engineering

Flinders University
TABLE 1

Studies Detecting Nontuberculosis Mycobacteria (NTM) From
Bovine Milk Products

Country     NTM                            Milk Type

Argentina   Mycobacterium avium            Commercially available
            subspecies paratuberculosis    pasteurized milk
            (MAP)

Austria     MAP in individual cow          Milk samples from individual
            samples but not in bulk tank   cows, raw and pasteurized
            milk                           bulk tank milk

Brazil      M. avium complex (MAC)         Raw milk from bulk tanks
                                           and individual animals

            Raw milk: M.                   Raw and pasteurized milk
            nonchromogenicum, M.
            peregrinum, M. smegmatis, M.
            neoaurum, M. fortuitum, M.
            flavescens, M. kansasii, and
            M. scrofulaceum
            Pasteurized milk: M.
            chelonae and M. peregrinum

            M. gordonae, M. fortuitum,     Raw milk from individual
            M. intracellulare, M.          and collective bulk tanks
            flavescens, M. duvalii, M.
            haemophilum, M. immunogenum,
            M. lentiflavum, M.
            mucogenicum, M.
            novocastrense, M.
            parafortuitum, M. smegmatis,
            M. terrae, and M. vaccae

            MAP                            Pasteurized milk

            M. simiae, M. kansasii, M.     Water buffalo raw milk
            flavescens, M. gordonae, and
            M. lentiflavum

            Raw milk: M. fortuitum,        Raw milk, UHT, and
            M. marinum, and M. gordonae    pasteurized milk
            UHT milk: No NTM detected
            Pasteurized milk: M.
            fortuitum, M. marinum, M.
            kansasii, and M. gordonae

Chile       MAP                            Bulk tank raw milk

Cyprus      MAP                            Raw milk from bulk tank and
                                           cheese originating from cow,
                                           sheep, goat, and
                                           mixed milks

            MAP and M. fortuitum           Bulk tank raw milk

Czech       MAP                            Powdered infant milk
Republic
            MAP                            Raw milk

            MAP                            Commercially pasteurized
                                           milk, locally pasteurized
                                           milk, and raw milk

Denmark     MAP                            Raw milk

European    MAP                            Powdered infant milk
Union
countries

India       MAP                            Pasteurized and
                                           unpasteurized milk

Iran        MAP                            Raw milk from individual
                                           milk, bulk tanks, and
                                           collection center bulk milk

            MAP                            Commercially available
                                           pasteurized milk

            MAP                            Raw milk from healthy cows
                                           and cows with Johne's
                                           disease symptoms

Iraq        MAP                            Powdered milk

Ireland     MAP                            Pasteurized and bulk raw
                                           milk

Italy       M. porcinum and MAP            Bulk raw milk

Switzer-    MAP                            Bulk tank raw milk
land

Tanzania    M. gordonae, M. phlei, M.      Raw milk
            fortuitum, M. smegmatis, M.
            flavescens, and MAC

            M. terrae, M. fortuitum, M.    Raw milk
            flavescens, M. gordonae, and
            M. smegmatis

Turkey      M. terrae, M. kansasii, M.     Raw milk
            haemophilum, M. agri, and
            two unidentified
            environmental Mycobacterium
            species

United      MAP                            Bulk raw milk and
Kingdom                                    commercially available
                                           pasteurized milk

            MAP                            Commercially available
                                           pasteurized milk

U.S.        MAP                            Commercially available
                                           pasteurized milk

            MAP                            Milk samples from
                                           individual raw bulk tank
                                           milk cows and

Country     NTM                            Detection
                                           Method

Argentina   Mycobacterium avium            Culture
            subspecies paratuberculosis
            (MAP)

Austria     MAP in individual cow          qPCR
            samples but not in bulk tank
            milk

Brazil      M. avium complex (MAC)         PCR

            Raw milk: M.                   Culture
            nonchromogenicum, M.
            peregrinum, M. smegmatis, M.
            neoaurum, M. fortuitum, M.
            flavescens, M. kansasii, and
            M. scrofulaceum
            Pasteurized milk: M.
            chelonae and M. peregrinum

            M. gordonae, M. fortuitum,     Culture
            M. intracellulare, M.
            flavescens, M. duvalii, M.
            haemophilum, M. immunogenum,
            M. lentiflavum, M.
            mucogenicum, M.
            novocastrense, M.
            parafortuitum, M. smegmatis,
            M. terrae, and M. vaccae

            MAP                            Culture

            M. simiae, M. kansasii, M.     Culture
            flavescens, M. gordonae, and
            M. lentiflavum

            Raw milk: M. fortuitum,        Culture
            M. marinum, and M. gordonae
            UHT milk: No NTM detected
            Pasteurized milk: M.
            fortuitum, M. marinum, M.
            kansasii, and M. gordonae

Chile       MAP                            qPCR

Cyprus      MAP                            Culture, qPCR,
                                           and combined
                                           phage PCR assay

            MAP and M. fortuitum           Culture and PCR

Czech       MAP                            qPCR
Republic
            MAP                            Culture and PCR

            MAP                            Culture

Denmark     MAP                            Culture and PCR

European    MAP                            PCR
Union
countries

India       MAP                            Culture and PCR

Iran        MAP                            Culture and qPCR

            MAP                            Culture and PCR

            MAP                            Culture and PCR

Iraq        MAP                            qPCR

Ireland     MAP                            Culture and
                                           IMS-PCR

Italy       M. porcinum and MAP            Culture

Switzer-    MAP                            PCR
land

Tanzania    M. gordonae, M. phlei, M.      Culture
            fortuitum, M. smegmatis, M.
            flavescens, and MAC

            M. terrae, M. fortuitum, M.    Culture
            flavescens, M. gordonae, and
            M. smegmatis

Turkey      M. terrae, M. kansasii, M.     Culture
            haemophilum, M. agri, and
            two unidentified
            environmental Mycobacterium
            species

United      MAP                            Culture and PCR
Kingdom
            MAP                            PCR

U.S.        MAP                            Culture

            MAP                            Culture

Country     NTM                            Reference

Argentina   Mycobacterium avium            Paolicchi et al., 2003
            subspecies paratuberculosis
            (MAP)

Austria     MAP in individual cow          Khol et al., 2013
            samples but not in bulk tank
            milk

Brazil      M. avium complex (MAC)         Bezerra et al., 2015

            Raw milk: M.                   Sgarioni et al., 2014
            nonchromogenicum, M.
            peregrinum, M. smegmatis, M.
            neoaurum, M. fortuitum, M.
            flavescens, M. kansasii, and
            M. scrofulaceum
            Pasteurized milk: M.
            chelonae and M. peregrinum

            M. gordonae, M. fortuitum,     Franco et al., 2013
            M. intracellulare, M.
            flavescens, M. duvalii, M.
            haemophilum, M. immunogenum,
            M. lentiflavum, M.
            mucogenicum, M.
            novocastrense, M.
            parafortuitum, M. smegmatis,
            M. terrae, and M. vaccae

            MAP                            Carvalho, Pietralonga,
                                           Schwarz, Faria, & Moreira,
                                           2012

            M. simiae, M. kansasii, M.     Jordao Junior, Lopes,
            flavescens, M. gordonae, and   David, Farache Filho, &
            M. lentiflavum                 Leite, 2009

            Raw milk: M. fortuitum,        Fujimura Leite et al., 2003
            M. marinum, and M. gordonae
            UHT milk: No NTM detected
            Pasteurized milk: M.
            fortuitum, M. marinum, M.
            kansasii, and M. gordonae

Chile       MAP                            Kruze, Monti, Schulze,
                                           Mella, & Leiva, 2013

Cyprus      MAP                            Botsaris et al., 2010

            MAP and M. fortuitum           Slana, Liapi, Moravkova,
                                           Kralova, & Pavlik, 2009

Czech       MAP                            Hruska, Slana, Kralik, &
Republic                                   Pavlik, 2011

            MAP                            Slana, Kralik, Kralova, &
                                           Pavlik, 2008

            MAP                            Ayele, Svastova, Roubal,
                                           Bartos, & Pavlik, 2005

Denmark     MAP                            Giese & Ahrens, 2000

European    MAP                            Hruska, Bartos, Kralik, &
Union                                      Pavlik, 2005
countries

India       MAP                            Shankar et al., 2010

Iran        MAP                            Hanifian, & Khani, 2016

            MAP                            Anzabi & Hanifian, 2012

            MAP                            Fathi, Sarkarati, Eslami,
                                           Rezavand, & Nourizadeh,
                                           2011

Iraq        MAP                            Hassan & Ali, 2012

Ireland     MAP                            O'Reilly et al., 2004

Italy       M. porcinum and MAP            Taddei et al., 2008

Switzer-    MAP                            Corti & Stephan, 2002
land

Tanzania    M. gordonae, M. phlei, M.      Mdegela et al., 2005
            fortuitum, M. smegmatis, M.
            flavescens, and MAC

            M. terrae, M. fortuitum, M.    Kazwala et al., 1998
            flavescens, M. gordonae, and
            M. smegmatis

Turkey      M. terrae, M. kansasii, M.     Konuk, Korcan, Dulgerbaki,
            haemophilum, M. agri, and      & Altindis, 2007
            two unidentified
            environmental Mycobacterium
            species

United      MAP                            Grant, Williams, Rowe, &
Kingdom                                    Muir, 2005

            MAP                            Millar et al., 1996

U.S.        MAP                            Ellingson et al., 2005

            MAP                            Pillai & Jayarao, 2002

IMS-PCR = immunomagnetic separation-polymerase chain reaction;
PCR = polymerase chain reaction; qPCR = quantitative polymerase chain
reaction; UHT = ultra-high temperature processing.
COPYRIGHT 2018 National Environmental Health Association
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:INTERNATIONAL PERSPECTIVES
Author:Whiley, Harriet; Adhikari, Shraddha; Keerthirathne, Thilini Piushani; Tohme, Tanya Caro
Publication:Journal of Environmental Health
Article Type:Report
Date:May 1, 2018
Words:5970
Previous Article:Evaluation of Nitrate Concentrations and Potential Sources of Nitrate in Private Water Supply Wells in North Carolina.
Next Article:All-Inclusive or a la Carte? Many Routes to Adopt the Model Aquatic Health Code.
Topics:

Terms of use | Privacy policy | Copyright © 2020 Farlex, Inc. | Feedback | For webmasters