期刊论文详细信息
BMC Microbiology
Antibiotic resistance, virulence determinants and production of biogenic amines among enterococci from ovine, feline, canine, porcine and human milk
Juan M Rodríguez2  Carmen Torres1  Miguel A Álvarez3  María Fernández3  Leonides Fernández2  Virginia Martín2  María López1  Antonio Maldonado-Barragán5  Irene Chico4  Victor Ladero3  Esther Jiménez4 
[1] Área de Bioquímica y Biología Molecular, Universidad de La Rioja, Logroño, Spain;Probisearch. c/Santiago Grisolía, Tres Cantos 2. 28760, Spain;Instituto de Productos Lácteos de Asturias (IPLA-CSIC), Paseo Río Linares s/n 33300, Villaviciosa, Spain;Departamento de Nutrición, Bromatología y Tecnología de los Alimentos, Universidad Complutense de Madrid, Ciudad Universitaria, Avda. Puerta de Hierro, Madrid s/n. 28040, Spain;Departamento de Biotecnología de Alimentos, Instituto de la Grasa-CSIC, Sevilla 41012, Spain
关键词: Biogenic amines;    Antibiotic resistance;    Virulence;    Mammals;    Milk;    Enterococcus;   
Others  :  1142410
DOI  :  10.1186/1471-2180-13-288
 received in 2013-07-04, accepted in 2013-12-04,  发布年份 2013
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【 摘 要 】

Background

Recent studies have shown that mammalian milk represents a continuous supply of commensal bacteria, including enterococci. The objectives of this study were to evaluate the presence of enterococci in milk of different species and to screen them for several genetic and phenotypic traits of clinical significance among enterococci.

Results

Samples were obtained from, at least, nine porcine, canine, ovine, feline and human healthy hosts. Enterococci could be isolated, at a concentration of 1.00 × 102 -1.16 × 103 CFU/ml, from all the porcine samples and, also from 85, 50, 25 and 25% of the human, canine, feline and ovine ones, respectively. They were identified as Enterococcus faecalis, Enterococcus faecium, Enterococcus hirae, Enterococcus casseliflavus and Enterococcus durans. Among the 120 initial enterococcal isolates, 36 were selected on the basis of their different PFGE profiles and further characterized. MLST analysis revealed a wide diversity of STs among the E. faecalis and E. faecium strains, including some frequently associated to hospital infections and novel STs. All the E. faecalis strains possessed some of the potential virulence determinants (cad, ccf, cob, cpd, efaAfs, agg2, gelE, cylA, espfs) assayed while the E. faecium ones only harboured the efaAfm gene. All the tested strains were susceptible to tigecycline, linezolid and vancomycin, and produced tyramine. Their susceptibility to the rest of the antimicrobials and their ability to produce other biogenic amines varied depending on the strain. Enterococci strains isolated from porcine samples showed the widest spectrum of antibiotic resistance.

Conclusions

Enterococci isolated from milk of different mammals showed a great genetic diversity. The wide distribution of virulence genes and/or antibiotic resistance among the E. faecalis and E. faecium isolates indicates that they can constitute a reservoir of such traits and a risk to animal and human health.

【 授权许可】

   
2013 Jiménez et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Butler JE: Immunoglobulins and immunocytes in animal milks. In Mucosal Immunology. Edited by Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR. New York: Academic Press; 1999.
  • [2]Kehrli ME Jr, Harp JA: Immunity in the mammary gland. Vet Clin North Am Food Anim Pract 2001, 17:495-516.
  • [3]Newburg DS, Walker WA: Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res 2007, 61:2-8.
  • [4]Stelwagen K, Carpenter E, Haigh B, Hodgkinson A, Wheeler TT: Immune components of bovine colostrum and milk. J Anim Sci 2009, 87(Suppl 13):3-9.
  • [5]Hurley WL, Theil PK: Perspectives on immunoglobulins in colostrum and milk. Nutrients 2011, 3:442-474.
  • [6]Heikkilä MP, Saris PEJ: Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 2003, 95:471-478.
  • [7]Martín R, Langa S, Reviriego C, Jiménez E, Marín ML, Xaus J, Fernández L, Rodríguez JM: Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 2003, 143:754-758.
  • [8]Martín R, Delgado S, Maldonado A, Jiménez E, Olivares M, Fernández L, Sobrino OJ, Rodríguez JM: Isolation of lactobacilli from sow milk and evaluation of their probiotic potential. J Dairy Res 2009, 76:418-425.
  • [9]Martín R, Olivares M, Pérez M, Xaus J, Torre C, Fernández L, Rodríguez JM: Identification and evaluation of the probiotic potential of lactobacilli isolated from canine milk. Vet J 2010, 185:193-198.
  • [10]Albesharat R, Ehrmann MA, Korakli M, Yazaji S, Vogel RF: Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst Appl Microbiol 2011, 34:148-155.
  • [11]Jin L, Hinde K, Tao L: Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta). J Med Primatol 2011, 40:52-58.
  • [12]Martín R, Heilig HG, Zoetendal EG, Jiménez E, Fernández L, Smidt H, Rodríguez JM: Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res Microbiol 2007, 158:31-37.
  • [13]Jiménez E, Delgado S, Maldonado A, Arroyo R, Albujar M, García N, Jariod M, Fernández L, Gómez A, Rodríguez JM: Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol 2008, 8:143.
  • [14]Hunt KM, Foster JA, Forney LJ, Schutte UM, Beck DL, Abdo Z, Fox LK, Williams JE, McGuire MK, McGuire MA: Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One 2011, 6:e21313.
  • [15]Reviriego C, Eaton T, Martín R, Jiménez E, Fernández L, Gasson MJ, Rodríguez JM: Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. J Hum Lact 2005, 21:131-137.
  • [16]Jiménez E, Delgado S, Fernández L, García N, Albujar M, Gómez A, Rodríguez JM: Assessment of the bacterial diversity of human colostrum and screening of staphylococcal and enterococcal populations for potential virulence factors. Res Microbiol 2008, 159:595-601.
  • [17]Borderon JC, Lionnet C, Rondeau C, Suc AI, Laugier J, Gold F: Current aspects of fecal flora of the newborn without antibiotherapy during the first 7 days of life: Enterobacteriaceae, enterococci, staphylococci. Pathol Biol 1996, 44:416-422.
  • [18]Jiménez E, Marín ML, Martín R, Odriozola JM, Olivares M, Xaus J, Fernández L, Rodríguez JM: Is meconium from healthy newborns actually sterile? Res Microbiol 2008, 159:187-193.
  • [19]Manson JM, Keis S, Smith JM, Cook GM: Characterization of a vancomycin-resistant Enterococcus faecalis (VREF) isolate from a dog with mastitis: further evidence of a clonal lineage of VREF in New Zealand. J Clin Microbiol 2003, 41:3331-3333.
  • [20]Kayser FH: Safety aspects of enterococci from the medical point of view. Int J Food Microbiol 2004, 88:255-262.
  • [21]Pomba C, Couto N, Moodley A: Treatment of a lower urinary tract infection in a cat caused by a multi-drug methicillin-resistant Staphylococcus pseudintermedius and Enterococcus faecalis. J Feline Med Surg 2010, 12:802-806.
  • [22]Eaton T, Gasson MJ: Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 2001, 67:1628-1635.
  • [23]Franz CMAP, Muscholl-Silberhorn AB, Yousif NMK, Vancanneyt M, Swings J, Holzapfel WH: Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol 2001, 67:4385-4389.
  • [24]Lebreton F, Van Schaik W, Manson McGuire A, Godfrey P, Griggs A, Mazumdar V, Corander J, Cheng L, Saif S, Young S, Zeng Q, Wortman J, Birren B, Willems RJL, Earl AM, Gilmore MS: Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. mBio 2013, 4:e00534-13.
  • [25]Teuber M: Veterinary use and antibiotic resistance. Curr Opin Microbiol 2001, 4:493-499.
  • [26]Hammerum AM, Lester CH, Heuer OE: Antimicrobial-resistant enterococci in animals and meat: a human health hazard? Foodborne Pathog Dis 2010, 7:1137-1146.
  • [27]Jensen LB, Ahrens P, Dons L, Jones RN, Hammerum AM, Aarestrup FM: Molecular analysis of Tn1546 in Enterococcus faecium isolated from animals and humans. J Clin Microbiol 1998, 36:437-442.
  • [28]Klare I, Konstabel C, Badstubner D, Werner G, Witte W: Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol 2003, 88:269-290.
  • [29]Ladero V, Calles-Enríquez M, Fernández M, Alvarez MA: Toxicological effects of dietary biogenic amines. Cur Nutr Food Sci 2010, 6:145-156.
  • [30]Dutka-Malen S, Evers S, Courvalin P: Detection of glycopeptides resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 1995, 33:24-27.
  • [31]Kullen MJ, Sanozky-Dawes RB, Crowell DC, Klaenhammer TR: Use of the DNA sequence of variable regions of the 16S rRNA gene for rapid and accurate identification of bacteria in the Lactobacillus acidophilus complex. J Appl Microbiol 2000, 89:511-516.
  • [32]Ruiz-Barba JL, Maldonado A, Jiménez-Díaz R: Small-scale total DNA extraction from bacteria and yeast for PCR applications. Anal Biochem 2005, 347:333-335.
  • [33]Jiménez E, Fernández L, Maldonado A, Martín R, Olivares M, Xaus J, Rodríguez JM: Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Appl Environ Microbiol 2008, 74:4650-4655.
  • [34]Ruiz-Garbajosa P, Bonten MJ, Robinson DA, Top J, Nallapareddy SR, Torres C, Cantón R, Baquero F, Murray BE, Del Campo R, Willems RJ: Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol 2006, 44:2220-2228.
  • [35]Homan WL, Tribe D, Poznanski S, Li M, Hogg M, Spalburg E, Van Embden JD, Willems RJ: Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol 2002, 40:1963-1971.
  • [36]Werner G, Fleige C, Geringer U, Van Schaik W, Klare I, Witte W: IS element IS16 as a molecular screening tool to identify hospital-associated strains of Enterococcus faecium. BMC Infect Dis 2011, 11:80.
  • [37]López M, Cercenado E, Tenorio C, Ruiz-Larrea F, Torres C: Diversity of clones and genotypes among vancomycin-resistant clinical Enterococcus isolates recovered in a Spanish Hospital. Microb Drug Resist 2012, 18:484-491.
  • [38]Lucas P, Lonvaud-funel A: Purification and partial gene sequence of the tyrosine decarboxylase of Lactobacillus brevis IOEB 9809. FEMS Microbiol Lett 2002, 211:85-89.
  • [39]Le Jeune C, Lonvaud-Funel A, Ten Brink B, Hofstra H, Van der Vossen JMBM: Development of a detection system for histidine decarboxylating lactic acid bacteria based on DNA probes, PCR and activity test. J Appl Bacteriol 1995, 78:316-326.
  • [40]Ladero V, Fernández M, Calles-Enríquez M, Sánchez-Llana E, Cañedo E, Martín MC, Alvarez MA: Is the production of the biogenic amines tyramine and putrescine a species-level trait in enterococci? Food Microbiol 2012, 30:132-138.
  • [41]García-Moruno E, Carrascosa AV, Muñoz R: A rapid and inexpensive method for the determination of biogenic amines from bacterial cultures by thin-layer chromatography. J Food Prot 2005, 68:625-629.
  • [42]CLSI. CLSI M100-S22: Performance Standards for Antimicrobial Susceptibility Testing; Twenty-second Informational Supplement. CLSI document M100-S22. Wayne, PA: Clinical and Laboratory Standards Institute; 2012.
  • [43]Ramos-Trujillo E, Pérez-Roth E, Méndez-Alvarez S, Claverie-Martín F: Multiplex PCR or simultaneous detection of enterococcal genes vanA and vanB and staphylococcal genes meca, ileS-2 and femB. Int Microbiol 2003, 6:113-115.
  • [44]Perichon B, Reynolds P, Courvalin P: VanD-type glycopeptide-resistant Enterococcus faecium BM 4339. Antimicrob Agents Chemother 1997, 41:2016-2018.
  • [45]Fines M, Perichon B, Reynolds P, Sahm DF, Courvalin P: VanE, a new type of acquired glycopeptide resistance in Enterococcus faecalis BM4405. Antimicrob Agents Chemother 1999, 43:2161-2164.
  • [46]McKessar SJ, Berry AM, Bell JM, Turnidge JD, Paton JC: Genetic characterization of vanG. A novel vancomycin resistance locus of Enterococcus faecalis. Antimicrob Agents Chemother 2000, 44:3224-3228.
  • [47]Solís G, De Los Reyes-Gavilan CG, Fernández N, Margolles A, Gueimonde M: Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 2010, 16:307-310.
  • [48]Little CL, De Louvois J: Health risks associated with unpasteurized goats’ and ewes’ milk on retail sale in England and Wales. A PHLS Dairy Products Working Group Study. Epidemiol Infect 1999, 122:403-408.
  • [49]Medina R, Katz M, Gonzalez S, Oliver G: Characterization of the lactic acid bacteria in ewe’s milk and cheese from northwest Argentina. J Food Prot 2001, 64:559-563.
  • [50]Kuch A, Willems RJL, Werner G, Coque TM, Hammerum AM, Sundsfjord A, Klare I, Ruiz-Garbajosa P, Simonsen GS, Van Luit-Asbroek M, Hryniewicz W, Sadowy E: Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J Antimicrob Chemother 2012, 67:551-558.
  • [51]Novais C, Freitas AR, Silveira E, Antunes P, Silva R, Coque TM, Peixe L: Spread of multidrug-resistant Enterococcus to animals and humans: an underestimated role for the pig farm environment. J Antimicrob Chemother 2013, 68:2746-2754.
  • [52]Ladero V, Fernández M, Alvarez MA: Isolation and identification of tyramine-producing enterococci from human fecal samples. Can J Microbiol 2009, 55:215-218.
  • [53]De Palencia PF, Fernández M, Mohedano ML, Ladero V, Quevedo C, Alvarez MA, López P: Role of tyramine synthesis by food-borne Enterococcus durans in adaptation to the gastrointestinal tract environment. Appl Environ Microbiol 2011, 77:699-702.
  • [54]Linares DM, Martín MC, Ladero V, Alvarez MA, Fernández M: Biogenic amines in dairy products. Crit Rev Food Sci Nutr 2011, 51:691-703.
  • [55]Aarestrup FM, Hasman H, Jensen LB, Moreno M, Herrero IA, Domínguez L, Finn M, Franklin A: Antimicrobial resistance among enterococci from pigs in three European countries. Appl Environ Microbiol 2002, 68:4127-4129.
  • [56]Phillips I, Casewell M, Cox T, De Groot B, Friis C, Jones R, Nightingale C, Preston R, Waddell J: Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J Antimicrob Chemother 2004, 53:28-52.
  • [57]Aarestrup FM: Characterization of glycopeptide-resistant Enterococcus faecium (GRE) from broilers and pigs in Denmark: genetic evidence that persistence of GRE in pig herds is associated with coselection by resistance to macrolides. J Clin Microbiol 2000, 38:2774-2777.
  • [58]Heuer OE, Hammerum AM, Collignon P, Wegener HC: Human health hazard from antimicrobial-resistant enterococci in animals and food. Clin Infect Dis 2006, 43:911-916.
  • [59]Sanciu G, Marogna G, Paglietti B, Cappuccinelli P, Leori G, Rappelli P: Outbreak of mastitis in sheep caused by multi-drug resistant Enterococcus faecalis in Sardinia, Italy. Epidemiol Infect 2012, 18:1-3.
  • [60]Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R: Cohabiting family members share microbiota with one another and with their dogs. Elife 2013, 2:e00458.
  • [61]Damborg P, Top J, Hendrickx AP, Dawson S, Willems RJ, Guardabassi L: Dogs are a reservoir of ampicillin-resistant Enterococcus faecium lineages associated with human infections. Appl Environ Microbiol 2009, 75:2360-2365.
  • [62]Tremblay CL, Charlebois A, Masson L, Archambault M: Characterization of hospital-associated lineages of ampicillin-resistant Enterococcus faecium from clinical cases in dogs and humans. Front Microbiol 2013, 4:245.
  • [63]Ghosh A, Dowd SE, Zurek L: Dogs leaving the ICU carry a very large multi-drug resistant enterococcal population with capacity for biofilm formation and horizontal gene transfer. PLoS One 2011, 6:e22451.
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