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An unusual PVL-positive MRSA strain in milk and dairy products from a region of South Italy
Journal of Global Antimicrobial Resistance 3 (2015) 151–152
Contents lists available at ScienceDirect
Journal of Global Antimicrobial Resistance journal homepage: www.elsevier.com/locate/jgar
Letter to the Editor An unusual PVL-positive MRSA strain in milk and dairy products from a region of South Italy Sir, Meticillin-resistant Staphylococcus aureus (MRSA) is a human pathogen of utmost importance both in healthcare settings and in the community, causing a wide range of diseases including pneumonia, sepsis, meningitis and skin and soft-tissue infection (SSTI). Differently from hospital-associated MRSA (HA-MRSA), community-associated MRSA (CA-MRSA) causes infections in otherwise healthy children or patients of young age and generally carries the Panton–Valentine leukocidin (PVL) genes. Recently, a new MRSA lineage, designated livestock-associated MRSA (LAMRSA), has been found to colonise pigs and other farm animals such as cattle and poultry. LA-MRSA has zoonotic capability and can colonise people in close contact with pigs and occasionally cause infections. These different MRSA subgroups can also be differentiated by molecular typing since they belong to different sequence types (STs) and clonal complexes and are associated with specific spa types; for instance, in Europe, LA-MRSA is mostly associated with ST398 and with a group of related spa types such as t011, t034 and t108 [1]. MRSA can contaminate food of animal origin, including milk. MRSA of different origins (both HA-MRSA and LA-MRSA) can cause bovine mastitis and hence contaminate milk and dairy products that can act as vehicles of transmission of MRSA to humans. We report the detection of an uncommon PVL-positive MRSA strain from milk and dairy products obtained from two farms in different provinces of Apulia region, South Italy. In one of these two farms, a classical LA-MRSA was also detected. Detection of MRSA was part of the routine monitoring programme performed on milk and dairy products in Italy. MRSA was isolated from several samples of spicy cheese in farm 1 and from samples of bovine milk and scamorza cheese in farm 2 obtained at different times during 2012. Identification of the isolates and of meticillin resistance was confirmed by PCR assays targeting nuc and mec, respectively. Detection of PVL genes, staphylococcal cassette chromosome mec (SCCmec) typing, spa typing and multilocus sequence typing (MLST) was performed applying the methods described previously [1]. In both farms, MRSA isolates contaminating cheese products were PVL-positive and belonged to a clone characterised by t355/ ST152/SCCmecV. In addition, in farm 2 the same strain was also found in bulk milk, along with a PVL-negative MRSA characterised by t899/ST398/SCCmecV, which corresponds to a typical LA-MRSA. The presence of LA-MRSA, a zoonotic organism, in milk and dairy products is not unprecedented, and indeed LA-MRSA ST398 has already been found in mozzarella cheese from the same region [2]. In contrast, the presence of PVL-positive MRSA is quite
unexpected, especially when it comes from a rather uncommon clone such as ST152. PVL-positive ST152 MRSA was first described in Slovenia in 2004 as a CA-MRSA, when it was isolated from a SSTI in a football player [3]. A PVL-positive MRSA with the t355/ST152 genotype, obtained from an immigrant child from Macedonia, was studied by microarray by Monecke et al. [4], who found that the strain lacked all of the enterotoxin genes, differently from other CA-MRSA strains. In 2008, in Genoa (Italy), t355/ST152 MRSA sustained a small outbreak in the intensive care unit of a children’s hospital, with the index case being a child from Albania [5]. In recent years, t355/ST152 has emerged as the most common PVL-positive CAMRSA in Austria [6]. This is one of the first reports describing PVL-positive MRSA isolates belonging to a CA-MRSA clonal lineage in dairy products and follows the recovery of one isolate with the same genotype in bovine milk in North Italy [7]. The CA-MRSA clonal lineage has probably emerged in the Balkans, spread to Austria and made sporadic appearances in Italy. The presence of farm workers from the Balkan countries in Apulia may suggest that the PVL-positive MRSA has been introduced in that area by colonised/infected farmers. Alternatively, one cannot exclude that this clone is a coloniser of cows in certain areas, although it has not been described in other reports studying mastitis milk. Investigating the colonisation of animals and workers in the two farms might contribute to elucidating this issue. Although LA-MRSA has been considered of low pathogenic potential for humans, CA-MRSA is prone to cause infections and epidemic clusters. Contamination of dairy products that, differently from meat products, are not normally subjected to cooking or heating before human consumption is rather worrisome, since it is more likely to represent an exposure risk for the consumer. Therefore, it is of the outmost importance not only to routinely screen dairy products for the presence of MRSA, but also to genotype the isolates to determine their likely origin and to guide control measures. Funding This study was supported in part by a grant from the Italian Ministry of Health (CCM) ‘Sorveglianza dell’antibiotico-resistenza in comunita`, nelle infezioni trasmesse dagli alimenti e in quelle di origine zoonosica’. Competing interests None declared. Ethical approval Not required.
http://dx.doi.org/10.1016/j.jgar.2015.03.002 2213-7165/ß 2015 International Society for Chemotherapy of Infection and Cancer. Published by Elsevier Ltd. All rights reserved.
152
Letter to the Editor / Journal of Global Antimicrobial Resistance 3 (2015) 151–152
References [1] Monaco M, Pedroni P, Sanchini A, Bonomini A, Indelicato A, Pantosti A. Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis 2013;13:258. [2] Crisetti E, Onni T, Sanchini A, Pantosti A, Tola S, La Salandra G. Detection of methicillin-resistant Staphylococcus aureus ST398 in mozzarella cheese in Italy. In: 22nd European Congress of Clinical Microbiology and Infectious Diseases (ECCMID); 2012 [poster 2362]. [3] Mu¨ller-Premru M, Strommenger B, Alikadic N, Witte W, Friedrich AW, Seme K, et al. New strains of community-acquired methicillin-resistant Staphylococcus aureus with Panton–Valentine leukocidin causing an outbreak of severe soft tissue infection in a football team. Eur J Clin Microbiol Infect Dis 2005;24:848–50. [4] Monecke S, Berger-Ba¨chi B, Coombs G, Holmes A, Kay I, Kearns A, et al. Comparative genomics and DNA array-based genotyping of pandemic Staphylococcus aureus strains encoding Panton–Valentine leukocidin. Clin Microbiol Infect 2007;13:236–49. [5] Ugolotti E, Bandettini R, Marchese A, Gualco L, Vanni I, Borzi L, et al. Molecular characterization of hospital-acquired methicillin-resistant Staphylococcus aureus strains in pediatric outbreaks using variable tandem repeat analysis with spa and ClfB typing. Diagn Microbiol Infect Dis 2011;69:213–7. [6] Krziwanek K, Luger C, Sammer B, Stumvoll S, Stammler M, Metz-Gercek S, et al. PVL-positive MRSA in Austria. Eur J Clin Microbiol Infect Dis 2007;26: 931–5.
[7] Benedetti V, Cremonesi P, Ferrari S, Castiglioni B, Fabbi M, Vicari N, et al. Staphylococcus aureus meticillino-resistenti (MRSA) da campioni di latte bovino. Large Anim Rev 2010;16:67–70.
Fabiola Mancini Monica Monaco Department of Infectious, Parasitic and Immune-mediated Diseases, Istituto Superiore di Sanita`, Rome I-00161, Italy Maria Grazia Basanisi Giovanna La Salandra Istituto Zooprofilattico Sperimentale di Puglia e Basilicata, Foggia, Italy Annalisa Pantosti* Department of Infectious, Parasitic and Immune-mediated Diseases, Istituto Superiore di Sanita`, Rome I-00161, Italy *Corresponding author E-mail address: [email protected] (A. Pantosti).
17 December 2014
Contents lists available at ScienceDirect
Journal of Global Antimicrobial Resistance journal homepage: www.elsevier.com/locate/jgar
Letter to the Editor An unusual PVL-positive MRSA strain in milk and dairy products from a region of South Italy Sir, Meticillin-resistant Staphylococcus aureus (MRSA) is a human pathogen of utmost importance both in healthcare settings and in the community, causing a wide range of diseases including pneumonia, sepsis, meningitis and skin and soft-tissue infection (SSTI). Differently from hospital-associated MRSA (HA-MRSA), community-associated MRSA (CA-MRSA) causes infections in otherwise healthy children or patients of young age and generally carries the Panton–Valentine leukocidin (PVL) genes. Recently, a new MRSA lineage, designated livestock-associated MRSA (LAMRSA), has been found to colonise pigs and other farm animals such as cattle and poultry. LA-MRSA has zoonotic capability and can colonise people in close contact with pigs and occasionally cause infections. These different MRSA subgroups can also be differentiated by molecular typing since they belong to different sequence types (STs) and clonal complexes and are associated with specific spa types; for instance, in Europe, LA-MRSA is mostly associated with ST398 and with a group of related spa types such as t011, t034 and t108 [1]. MRSA can contaminate food of animal origin, including milk. MRSA of different origins (both HA-MRSA and LA-MRSA) can cause bovine mastitis and hence contaminate milk and dairy products that can act as vehicles of transmission of MRSA to humans. We report the detection of an uncommon PVL-positive MRSA strain from milk and dairy products obtained from two farms in different provinces of Apulia region, South Italy. In one of these two farms, a classical LA-MRSA was also detected. Detection of MRSA was part of the routine monitoring programme performed on milk and dairy products in Italy. MRSA was isolated from several samples of spicy cheese in farm 1 and from samples of bovine milk and scamorza cheese in farm 2 obtained at different times during 2012. Identification of the isolates and of meticillin resistance was confirmed by PCR assays targeting nuc and mec, respectively. Detection of PVL genes, staphylococcal cassette chromosome mec (SCCmec) typing, spa typing and multilocus sequence typing (MLST) was performed applying the methods described previously [1]. In both farms, MRSA isolates contaminating cheese products were PVL-positive and belonged to a clone characterised by t355/ ST152/SCCmecV. In addition, in farm 2 the same strain was also found in bulk milk, along with a PVL-negative MRSA characterised by t899/ST398/SCCmecV, which corresponds to a typical LA-MRSA. The presence of LA-MRSA, a zoonotic organism, in milk and dairy products is not unprecedented, and indeed LA-MRSA ST398 has already been found in mozzarella cheese from the same region [2]. In contrast, the presence of PVL-positive MRSA is quite
unexpected, especially when it comes from a rather uncommon clone such as ST152. PVL-positive ST152 MRSA was first described in Slovenia in 2004 as a CA-MRSA, when it was isolated from a SSTI in a football player [3]. A PVL-positive MRSA with the t355/ST152 genotype, obtained from an immigrant child from Macedonia, was studied by microarray by Monecke et al. [4], who found that the strain lacked all of the enterotoxin genes, differently from other CA-MRSA strains. In 2008, in Genoa (Italy), t355/ST152 MRSA sustained a small outbreak in the intensive care unit of a children’s hospital, with the index case being a child from Albania [5]. In recent years, t355/ST152 has emerged as the most common PVL-positive CAMRSA in Austria [6]. This is one of the first reports describing PVL-positive MRSA isolates belonging to a CA-MRSA clonal lineage in dairy products and follows the recovery of one isolate with the same genotype in bovine milk in North Italy [7]. The CA-MRSA clonal lineage has probably emerged in the Balkans, spread to Austria and made sporadic appearances in Italy. The presence of farm workers from the Balkan countries in Apulia may suggest that the PVL-positive MRSA has been introduced in that area by colonised/infected farmers. Alternatively, one cannot exclude that this clone is a coloniser of cows in certain areas, although it has not been described in other reports studying mastitis milk. Investigating the colonisation of animals and workers in the two farms might contribute to elucidating this issue. Although LA-MRSA has been considered of low pathogenic potential for humans, CA-MRSA is prone to cause infections and epidemic clusters. Contamination of dairy products that, differently from meat products, are not normally subjected to cooking or heating before human consumption is rather worrisome, since it is more likely to represent an exposure risk for the consumer. Therefore, it is of the outmost importance not only to routinely screen dairy products for the presence of MRSA, but also to genotype the isolates to determine their likely origin and to guide control measures. Funding This study was supported in part by a grant from the Italian Ministry of Health (CCM) ‘Sorveglianza dell’antibiotico-resistenza in comunita`, nelle infezioni trasmesse dagli alimenti e in quelle di origine zoonosica’. Competing interests None declared. Ethical approval Not required.
http://dx.doi.org/10.1016/j.jgar.2015.03.002 2213-7165/ß 2015 International Society for Chemotherapy of Infection and Cancer. Published by Elsevier Ltd. All rights reserved.
152
Letter to the Editor / Journal of Global Antimicrobial Resistance 3 (2015) 151–152
References [1] Monaco M, Pedroni P, Sanchini A, Bonomini A, Indelicato A, Pantosti A. Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect Dis 2013;13:258. [2] Crisetti E, Onni T, Sanchini A, Pantosti A, Tola S, La Salandra G. Detection of methicillin-resistant Staphylococcus aureus ST398 in mozzarella cheese in Italy. In: 22nd European Congress of Clinical Microbiology and Infectious Diseases (ECCMID); 2012 [poster 2362]. [3] Mu¨ller-Premru M, Strommenger B, Alikadic N, Witte W, Friedrich AW, Seme K, et al. New strains of community-acquired methicillin-resistant Staphylococcus aureus with Panton–Valentine leukocidin causing an outbreak of severe soft tissue infection in a football team. Eur J Clin Microbiol Infect Dis 2005;24:848–50. [4] Monecke S, Berger-Ba¨chi B, Coombs G, Holmes A, Kay I, Kearns A, et al. Comparative genomics and DNA array-based genotyping of pandemic Staphylococcus aureus strains encoding Panton–Valentine leukocidin. Clin Microbiol Infect 2007;13:236–49. [5] Ugolotti E, Bandettini R, Marchese A, Gualco L, Vanni I, Borzi L, et al. Molecular characterization of hospital-acquired methicillin-resistant Staphylococcus aureus strains in pediatric outbreaks using variable tandem repeat analysis with spa and ClfB typing. Diagn Microbiol Infect Dis 2011;69:213–7. [6] Krziwanek K, Luger C, Sammer B, Stumvoll S, Stammler M, Metz-Gercek S, et al. PVL-positive MRSA in Austria. Eur J Clin Microbiol Infect Dis 2007;26: 931–5.
[7] Benedetti V, Cremonesi P, Ferrari S, Castiglioni B, Fabbi M, Vicari N, et al. Staphylococcus aureus meticillino-resistenti (MRSA) da campioni di latte bovino. Large Anim Rev 2010;16:67–70.
Fabiola Mancini Monica Monaco Department of Infectious, Parasitic and Immune-mediated Diseases, Istituto Superiore di Sanita`, Rome I-00161, Italy Maria Grazia Basanisi Giovanna La Salandra Istituto Zooprofilattico Sperimentale di Puglia e Basilicata, Foggia, Italy Annalisa Pantosti* Department of Infectious, Parasitic and Immune-mediated Diseases, Istituto Superiore di Sanita`, Rome I-00161, Italy *Corresponding author E-mail address: [email protected] (A. Pantosti).
17 December 2014