Staphylococcus aureus is a Gram-positive bacterium affecting human health, and a major cause of skin infections, endocarditis, meningitis, and sepsis. Methicillin-resistant S. aureus (MRSA) is a worldwide health concern, occurs in food animals, is consistently found in swine, and improved strategies are needed to ensure the removal of MRSA from food products. A total of 164 S. aureus strains were isolated from swine mandibular lymph node tissue, commercial pork sausage meat, and feces. These strains were tested for methicillin-resistance, and 7 of the strains isolated from the mandibular lymph node tissue and pork sausage meat were resistant to cefoxitin and oxacillin, and tested positive for staph specific rRNA and for the mecA gene and are therefore, MRSA strains. An intracellular MRSA contamination of 8.2% within swine lymph node tissue and 5.8% MRSA contamination in pork sausage meat was demonstrated. Lymph node tissue may be utilized in producing pork sausage; therefore, the prevalence of MRSA in final pork products may not only be caused by surface contamination, but by internal tissue infection. The strains were tested for susceptibility to six organic acids (OAs) citric, L-lactic, butyric, acetic, propionic, and formic acid. The pH was determined at each of the minimum inhibitory concentrations (MICs) observed for the S. aureus strains. The Henderson-Hasselbalch equation was used to calculate the ratio of the undissociated to dissociated OA concentrations, and the molar concentrations of each were calculated from the total OA present and the ratio. Inhibition of S. aureus did not correlate with pH or the undissociated OA concentrations, but it did correlate with the dissociated OA concentrations. A dissociated OA concentration of 21 mM was successful for inhibiting the S. aureus strains tested. Studies must be conducted in vivo to confirm this concentration value. Acetic, butyric, formic, and propionic acid were the most effective OAs tested against S. aureus.
| Published in | International Journal of Microbiology and Biotechnology (Volume 5, Issue 4) |
| DOI | 10.11648/j.ijmb.20200504.12 |
| Page(s) | 165-183 |
| Creative Commons |
This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited. |
| Copyright |
Copyright © The Author(s), 2020. Published by Science Publishing Group |
Acetic Acid, Citric Acid, Formic Acid, L-Lactic Acid, Molar Minimum inhibitory Concentrations (MICMs), Organic Acids, Propionic Acid, Staphylococcus aureus, Susceptibility, Swine
| [1] | Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, Beach M and the SENTRY Participants Group (2001) Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clin. Infect. Dis. 32 (Suppl. 2): S114–132. doi: 10.1086/320184. |
| [2] | Spahich NA, Vitko NP, Thurlow LR, Temple B and Richardson AR (2016) Staphylococcus aureus lactate- and malate-quinone oxidoreductases contribute to nitric oxide resistance and virulence. Mol. Microbiol. 100: 759–773. doi: 10.1111/mmi.13347. |
| [3] | Kluytmans J, van Belkum A and Verbrugh H (1997) Nasal carriage of Staphylococcus aureus: Epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10: 505–520. doi: 10.1128/CMR.10.3. 505. |
| [4] | Gould IM (2009) Antibiotics, skin and soft tissue infection and methicillin-resistant Staphylococcus aureus: Cause and effect. Int. J. Antimicrob. Agents 34 (Suppl. 1): S8–S11. doi: 10.1016/ S0924-8579(09)70542-4. |
| [5] | Saïd-Salim B, Dunman PM, McAleese FM, Macapagal D, Murphy E, McNamara PJ, Arvidson S, Foster TJ, Projan SJ and Kreiswirth BN (2003) Global regulation of Staphylococcus aureus genes by Rot. J. Bacteriol. 185: 610–619. doi: 10.1128/JB.185.2.610-619.2003. |
| [6] | Otero MC, Morelli L and Nader-Macías ME (2006) Probiotic properties of vaginal lactic acid bacteria to prevent metritis in cattle. Lett. Appl. Microbiol. 43: 91–97. doi: 10.1111/j.1472-765X.2006.01914.x. |
| [7] | CDC (2020) Foodborne germs and illnesses. Available at: https://www.cdc.gov/foodsafety/foodborne-germs.html (Accessed on: 17 July 2020). |
| [8] | National Center for Case Methicillin resistant Staphylococcus aureus (MRSA) (2020) Available at: https://sciencecases.lib. buffalo.edu/files/Supplemental/UploadFolder/skin_graft.pdf (Accessed on: 06 October 2020). |
| [9] | Verstappen KM, Willems E, Fluit AC, Duim B, Martens M and Wagenaar JA (2017) Staphylococcus aureus nasal colonization differs among pig lineages and is associated with the presence of other staphylococcal species. Front. Vet. Sci. 4: 97. doi: 10.3389/fvets.2017.00097. |
| [10] | Lassok B and Tenhagen B-A (2013) From pig to pork: Methicillin-resistant Staphylococcus aureus in the pork production chain. J. Food Prot. 76: 1095–1108. doi: 10.4315/ 0362-028XJFP-12-341. |
| [11] | Leonard FC and Markey BK (2008) Meticillin-resistant Staphylococcus aureus in animals: A review. Vet. J. 175: 27–36. doi: 10.1016/j.tvjl.2006.11.008. |
| [12] | Cuny C, Friedrich A, Kozytska S, Layer F, Nübel U, Ohlsen K, Strommenger B, Walther B, Wieler L and Witte W (2010) Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J. Med. Microbiol. 300: 109–117. doi: 10.1016/j.ijmm.2009.11.002. |
| [13] | Weese JS (2010) Methicillin-resistant Staphylococcus aureus in animals. ILAR J. 51: 233–244. doi: 10.1093/ilar. 51.3.233. |
| [14] | Nadimpalli M, Stewart JR, Pierce E, Pisanic N, Love DC, Hall D, Larsen J, Carroll KC, Tekle T, Perl TM, et al. (2016) Livestock-associated, antibiotic-resistant Staphylococcus aureus nasal carriage and recent skin and soft tissue infection among industrial hog operation workers. PLoS ONE 11: e0165713. doi: 10.1371/journal.pone0165713. |
| [15] | Carrel M, Schweizer ML, Sarrazin MV, Smith TC and Perencevich EN (2014) Residential proximity to large numbers of swine in feeding operations is associated with increased risk of methicillin-resistant Staphylococcus aureus colonization at time of hospital admission in rural Iowa veterans. Infect. Control Hospital Epidemiol. 35: 190–192. doi: 10.1086/674860. |
| [16] | Parisi A, Caruso M, Normanno G, Latorre L, Miccolupo A, Fraccalvieri R, Intini F, Manginelli T and Santagada G (2019) MRSA in swine, farmers and abattoir workers in Southern Italy. Food Microbiol. 82: 287–293. https://doi.org/10.1016/j. fm.2019.03.003. |
| [17] | Cuny C, Wieler LH and Witte W (2015) Livestock-associated MRSA: The impact on humans. Antibiotics 4: 521–543. doi: 10.3390/antibiotics404521. |
| [18] | Slifierz MJ, Friendship RM and Weese JS (2015) Methicillin-resistant Staphylococcus aureus in commercial swine herds is associated with disinfectant and zinc usage. Appl. Environ. Microbiol. 81: 2690–2695. doi: 10.1128/AEM.00036-15. |
| [19] | Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM, Male MJ, Martin HW, Molla BZ, Sreevatsan S, Thakur S, et al. (2013) Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS ONE 8: e63704. doi: 10.1371/journal. pone.0063704. |
| [20] | Davis MF, Pisanic N, Rhodes SM, Brown A, Keller H, Nadimpalli M, Christ A, Ludwig S, Ordak C, Spicer K, et al. (2018) Occurrence of Staphylococcus aureus in swine and swine workplace environments on industrial and antibiotic-free hog operations in North Carolina, USA: A one health pilot study. Environ. Res. 163: 88–96. doi: 10.1016/j.envres.2017. 12.010. |
| [21] | Wardyn SE, Forshey BM, Farina SA, Kates AE, Nair R, Quick MK, Wu JY, Hanson BM, O’Malley SM, Shows HW, et al. (2015) Swine farming is a risk factor for infection with high prevalence of carriage of multidrug-resistant Staphylococcus aureus. Clin. Infect. Dis. 61: 59–66. doi: 10.1093/cid/civ234. |
| [22] | Rinsky JL, Nadimpalli M, Wing S, Hall D, Baron D, Price LB, Larsen J, Stegger M, Stewart J and Heaney CD (2013) Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in North Carolina. PLoS ONE 8: e67641. doi: 10.1371/journal.pone.0067641. |
| [23] | Smith TC and Wardyn SE (2015) Human infections with Staphylococcus aureus CC398. Cur. Environ. Health Rpt. 2: 41–51. doi: 10.1007/s40572-014-0034-8. |
| [24] | Ye X, Fan Y, Wang X, Liu W, Yu H, Zhou J, Chen S and Yao Z (2016) Livestock-associated methicillin and multidrug resistant S. aureus in humans is associated with occupational pig contact, not pet contact. Sci Rep. 6: 19184. doi: 10.1038/ srep19184. |
| [25] | Hatcher SM, Rhodes SM, Stewart JR, Silbergeld E, Pisanic N, Larsen J, Jiang S, Krosche A, Hall D, Carroll KC, et al. (2017) The prevalence of antibiotic-resistant Staphylococcus aureus nasal carriage among industrial hog operation workers, community residents, and children living in their households: North Carolina, USA. Environ. Health Perspect. 125: 560–569. doi: 10.1289/EHP35. |
| [26] | Nehme B, Létourneau V, Forster RJ, Veillette M and Duchaine C (2008) Culture-independent approach of the bacterial bioaerosol diversity in the standard swine confinement buildings, and assessment of the seasonal effect. Environ. Microbiol. 10: 665–675. doi: 10.1111/j.1462-2920.2007.01489.x. |
| [27] | Cole D, Todd L and Wing S (2000) Concentrated swine feeding operations and public health: A review of occupational and community health effects. Environ. Health Perspect. 108: 685–699. doi: 10.1289/ehp. 00108685. |
| [28] | Beresin GA, Wright JM, Rice GE and Jagai JS (2017) Swine exposure and methicillin-resistant Staphylococcus aureus infection among hospitalized patients with skin and soft tissue infections in Illinois: A ZIP code-level analysis. Environ. Res. 159: 46–60. doi: 10.1016/j.envres.2017.07.037. |
| [29] | Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD and Scarpino PV (2006) Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ. Health Perspect. 114: 1032–1037. doi: 10.1289/ehp.8910. |
| [30] | Schulz J, Friese A, Klees S, Tenhagen BA, Fetsch A, Rösler U and Hartung J (2012) Longitudinal study of the contamination of air and of soil surfaces in the vicinity of pig barns by livestock-associated methicillin-resistant Staphylococcus aureus. Appl. Environ. Microbiol. 78, 5666–5671. doi: 10.1128/AEM.00550-12. |
| [31] | Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin Y-F, Yannarell AC, Maxwell S and Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J. Environ. Qual. 38, 1086–1108. doi: 10.2134/jeq2008.0128. |
| [32] | Heuer H, Schmitt H and Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr. Opin. Microbiol. 14, 236–243. doi: 10.1016/j.mib.2011. 04.009. |
| [33] | Casey JA, Curriero FC, Cosgrove SE, Nachman KE and Schwartz BS (2013) High-density livestock operations, crop field application of manure, and risk of community-associated methicillin-resistant Staphylococcus aureus infection in Pennsylvania. JAMA Intern. Med. 173: 1980–1990. doi: 10. 1001/jamainternmed.2013.10408. |
| [34] | Pu S, Han F and Ge B (2009) Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl. Environ. Microbiol. 75, 265–267. doi: 10.1128/AEM.01110-08. |
| [35] | O’Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE, Forshey BM, Kulick ME, Wallinga DB, Smith TC (2012) MRSA in conventional and alternative retail pork products. PLoS ONE, 7: e30092. doi: 10.1371/journal.pone. 0030092. |
| [36] | Kluytmans J, van Leeuwen W, Goessens W, Hollis R, Messer S, Herwaldt L, Bruining H, Heck M, Rost J, van Leeuwen N, et al. (1995) Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by pheno- and genotyping. J. Clin. Microbiol. 33: 1121–1128. PMCID: PMC228116, PMID: 7615715. |
| [37] | Jones TF, Kellum ME, Porter SS, Bell M and Schaffner W (2002) An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg. Infect. Dis. 8: 82–84. doi: 10.3201/eid0801.010174. |
| [38] | Buchanan RL (1997) Identifying and controlling emerging foodborne pathogens: Research needs. Emerg. Infect. Dis. 3: 517–521. doi: 10.3201/eid0304.970416. |
| [39] | Wachsmuth IK, Sparling PH, Barrett TJ and Potter ME (1997) Enterohemorrhagic Escherichia coli in the United States. FEMS Immunol. Med. Microbiol. 18: 233–239. doi: 10.1111/j. 1574-695X.1997.tb01051.x. |
| [40] | Hinton MH and Corry JEL (1999) The decontamination of carcass meat. In: Poultry Meat Science, Richardson RI and Mead GC (Eds), Wallingford; Oxford, UK, CAB1 Publishing, pp. 285–295. |
| [41] | Raftari M, Jalilian FA, Abdulamir AS, Son R, Sekawi Z and Fatimah AB (2009) Effect of organic acids on Escherichia coli O157:H7 and Staphylococcus aureus contaminated meat. Microbiol J. 3: 121–127. doi: 10.2174/18742858009030101 21. |
| [42] | Raftari M, Aziz Jalilian F, Abdulamir AS, Ghafurian S, Radu S, Sekawi Z and Abu Bakar F (2011) Optimized antibacterial measures against Escherichia coli O157:H7 and Staphylococcus aureus. Afr. J. Microbiol. Res. 5: 3113–3121. doi: 10.5897/AJMR10.099. |
| [43] | Mani-López E, Garci HS and López-Malo A (2012) Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res. Int. 45: 713–721. doi: 10.1016/j. foodres.2011.04.043. |
| [44] | Epling LK, Carpenter JA and Blankenship LC (1993) Prevalence of Campylobacter spp. and Salmonella spp. on pork carcasses and the reduction effected by spraying with lactic acid. J. Food Prot. 56, 536–537. doi: 10.4315/0362-028X-56.6.536. |
| [45] | Castillo A, Lucia LM, Roberson DB, Stevenson TH, Mercado I and Acuff GR (2001) Lactic acid sprays reduce bacterial pathogens on cold beef carcass surfaces and in subsequently produced ground beef. J. Food Prot. 64: 58–62. doi: 10.4315/ 0362-028X-64.1.58. |
| [46] | Departments of Pennsylvania State University, Texas Tech University, and Washington State University (2005) Antimicrobial spray treatments for red meat carcasses processed in very small meat establishments. Available at: http://meathaccp.wisc.edu/validation/assets/acid_spray_intervention_booklet_from_penn_state_2005.pdf (Accessed on: 22 July 2020). |
| [47] | Reynolds AE Jr (2005) Utilization of spray wash with organic acids (peroxyacetic acid and lactic acid) and chlorinated wash in combination, utilizing direct application methods, for pathogen reduction on pork and beef carcasses in small and very small meat processing plants (revised 8/24/2005). Available at: http://www.fsis.usda.gov/wps/wcm/connect/acc8bddb-eb64-4ea2-82eb-565cf337691a/New_Technology_C29_Summary_FY2003.pdf?MOD=AJPERES (Accessed on: 22 July 2020). |
| [48] | Dickson JS, Hardin MD and Acuff GR (1996) Organic acid rinses. In: Microbiology Intervention Methods, Proceedings of the 49th Annual Reciprocal Meat Conference, American Meat Science Association, pp. 129–131. Available at: https://meatscience.org/docs/default-source/publications-resources/rmc/1996/organic-acid-rinses.pdf?sfvrsn=2 (Accessed on: 18 September 2020). |
| [49] | Dickson JS and Acuff GR (2017) Maintaining the safety and quality of beef carcass meat. In: Ensuring Safety and Quality in the Production of Beef. Vol. 1: Safety. Acuff, G. R.; Dickson, J. S. (Eds.), Burleigh Dodds Science Publishing: Sawston, Cambridge, UK. Available at: https://lib.dr.iastate.edu/cgi/viewcontent.cgi?article=1354&context=ans_pubs (Accessed on: 22 July 2020). |
| [50] | Ricke SC (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 82: 632–639. doi: 10.1093/ps/82.4.632. |
| [51] | Minor TE and Marth EH (1970) Growth of Staphylococcus aureus in acidified pasteurized milk. J. Milk Food Technol. 33: 516–520. doi: 10.4315/0022-2747-33.11.516. |
| [52] | Sofos JN and Busta FF (1981) Antimicrobial activity of sorbate. J. Food Prot. 44: 614–622. doi: 10.4315/0362-028X-44.8.614. |
| [53] | Blocher JC, Busta FF and Sofos JN (1982) Influence of potassium sorbate and pH on ten strains of type A and B Clostridium botulinum. J. Food Sci. 47: 2028–2032. doi: 10.1111/j.1365-2621.1982.tb12938.x. |
| [54] | Ray B and Sandine WE (1992) Acetic, propionic, and lactic acids of starter culture bacteria as biopreservatives. In Food Biopreservatives of Microbial Origin; Ray, B., Daeschel, M., Eds.; CRC Press, Inc.; Boca Raton, FL, USA, pp. 103–136. |
| [55] | Breidt F Jr, Hayes JS and McFeeters RF (2004) Independent effects of acetic acid and pH on survival of Escherichia coli in simulated acidified pickle products. J. Food Prot. 67: 12–18. doi: 10.4315/0362-028x-67.1.12. |
| [56] | Leeson S (2007) Balancing science versus societal issues in poultry nutrition. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 2: 071. doi: 10.1079/PAVSNNR20072071. |
| [57] | Ghosh HK, Halder G, Samanta G and Koley S (2008) Effect of dietary supplementation of organic acid and mannan oligosaccharide on the plasma minerals and carcass traits of Japanese quail (Coturnix coturnix japonica). Res. J. Vet. Sci. 1: 44–49. doi: 10.3923/rjvs.2008.44.49. |
| [58] | Van Deun K, Haesebrouch F, Van Immerseel F, Ducatelle R and Pasmans F (2008) Short-chain fatty acids and L-lactate as feed additives to control Campylobacter jejuni infections in broilers. Avian Pathol. 37: 379–383. doi: 10.1080/03079450802216603. |
| [59] | Bushell FML, Tonner PD, Jabbari S, Schmid, AK and Lund PA (2019) Synergistic impacts of organic acids and pH on growth of Pseudomonas aeruginosa: A comparison of parametric and Bayesian non-parametric methods to model growth. Front. Microbiol. 9: 3196. doi: 10.3389/fmicb.2018. 03196. |
| [60] | Presser KA, Ross T and Ratkowsky DA (1998) Modelling the growth limits (growth/no growth interface) of Escherichia coli as a function of temperature, pH, lactic acid concentration, and water activity. Appl. Environ. Microbiol. 64: 1773–1779. PMCID: PMC106229; PMID: 9572950. |
| [61] | Carpenter CE and Broadbent JR (2009) External concentration of organic acid anions and pH: Key independent variables for studying how organic acids inhibit growth of bacteria in mildly acidic foods. J. Food Sci. 74: R12–R15. doi: 10.1111/j.1750-3841.2008.00994.x. |
| [62] | Beier RC, Harvey RB, Hernandez CA, Hume ME, Andrews K, Droleskey RE, Davidson MK, Bodeis-Jones S, Young S, Duke SE, et al. (2018) Interactions of organic acids with Campylobacter coli from swine. PLoS ONE 13: e0202100. doi: 10.1371/journal.pone.0202100. |
| [63] | Beier RC, Poole TL, Brichta-Harhay DM, Anderson RC, Bischoff KM, Hernandez CA, Bono JL, Arthur TM, Nagaraja TG, Crippen TL, et al. (2013) Disinfectant and antibiotic susceptibility profiles of Escherichia coli O157:H7 strains from cattle carcasses, feces, and hides and ground beef from the United States. J. Food Prot. 76: 6–17. doi: 10.4315/0362-028X.JFP-12-253. |
| [64] | Beier RC, Foley SL, Davidson MK, White DG, McDermott PF, Bodeis-Jones S, Zhao S, Andrews K, Crippen TL, Sheffield CL, et al. (2014) Characterization of antibiotic and disinfectant susceptibility profiles among Pseudomonas aeruginosa veterinary isolates recovered during 1994–2003. J. Appl. Microbiol. 118: 326–342. doi: 10.1111/jam.12707. |
| [65] | Beier RC, Franz E, Bono JL, Mandrell RE, Fratamico PM, Callaway TR, Andrews K, Poole TL, Crippen TL, Sheffield CL, et al. (2016) Disinfectant and antimicrobial susceptibility profiles of the big six non-O157 Shiga toxin-producing Escherichia coli strains from food animals and humans. J. Food Prot. 79: 1355–1370. doi: 10.4315/0362-028X.JFP-15-600. |
| [66] | Beier RC, Callaway TR, Andrews K, Poole TL, Crippen TL, Anderson RC and Nisbet DJ (2017) Interactions of organic acids with Salmonella strains from feedlot water-sprinkled cattle. J. Food Chem. Nanotechnol. 3: 60–66. doi: 10.17756/ jfcn.2017-038. |
| [67] | Beier RC, Byrd JA, Caldwell D, Andrews K, Crippen TL, Anderson RC and Nisbet DJ (2019) Inhibition and interactions of Campylobacter jejuni from broiler chicken houses with organic acids. Microorganisms 7: 223. doi: 10.3390/microorganisms7080223. |
| [68] | Beier RC, Harvey RB, Poole TL, Hume ME, Crippen TL, Highfield LD, Alali WQ, Andrews K, Anderson RC and Nisbet DJ (2018) Interactions of organic acids with vancomyin-resistant Enterococcus faecium isolated from community wastewater in Texas. Appl. Microbiol. 126: 480–488. doi: 10.1111/jam.14145. |
| [69] | Alakomi H-L, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K and Helander IM (2000) Lactic acid permeabilizes Gram-negative bacteria by disrupting the outer membrane. Appl. Environ. Microbiol. 66: 2001–2005. doi: 10.1128/AEM.66.5.2001-2005.2000. |
| [70] | Dallenne C, Da Costa A, Decré D, Favier C and Arlet G (2010) Development of a set of multiplex PCR assays for the detection of genes encoding important -lactamases in Enterobacteriaceae. J. Antimicrob. Chemother. 65: 490–495. doi: 10.1093/jac/dkp498. |
| [71] | Mason WJ, Blevins JS, Beenken K, Wibowo N, Ojha N and Smeltzer MS (2001) Multiplex PCR protocol for the diagnosis of staphylococcal infection. J. Clin. Microbiol. 39: 3332–3338. doi: 10.1128/JCM.39.3332-3338.2001. |
| [72] | Clinical and Laboratory Standards Institute (CLSI) (2018) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 11th ed. CLSI approved standard, M07. Clinical and Laboratory Standards Institute, Wayne, PA, USA. |
| [73] | Andrews JM (2001) Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48 (Suppl. S1): 5–16. doi: 10.1093/jac/48.suppl_1.5. |
| [74] | Helmenstine AM (2019) Henderson-Hasselbalch equation and example. Available at: http://chemistry.about.com/od/ acidsbase1/a/hendersonhasselbalch.htm (Accessed on: 4 August 2020). |
| [75] | Gill CO and Bryant J (1992) The contamination of pork with spoilage bacteria during commercial dressing, chilling and cutting of pig carcasses. Int. J. Food Microbiol. 16: 51–62. doi: 10.1016/0168-1605(92)90125-M. |
| [76] | Sörqvist S and Danielsson Tham M-L (1987) Bacterial contamination of the scalding water during vat scalding of pigs. Fleischwirtschaft Int. 2: 39–43. URN: urn:nbn:se:oru-58128. |
| [77] | Gill CO, McGinnis DS, Bryant J and Chabot B (1995) Decontamination of commercial polished pig carcasses with hot water. Food Microbiol. 12: 337–344. doi: 10.1016/S0740-0020(95)80090-5. |
| [78] | Beneke B, Klees S, Stührenberg B, Fetsch A and Kraushaar B Tenhagen B-A (2011) Prevalence of methicillin-resistant Staphylococcus aureus in a fresh meat pork production chain. J. Food Prot. 74: 126–129. doi: 10.4315/0362-028X.JFP-10-250. |
| [79] | Shaheen BW, Miller ME and Oyarzabal OA (2007) In vitro survival at low pH and acid adaptation response of Campylobacter jejuni and Campylobacter coli. J. Food Saf. 27: 326–343. doi: 10.1111/j.1745-4565.2007. 00083.x. |
| [80] | Mann E, Dzieciol M, Pinior B, Neubauer V, Metzler-Zebeli BU, Wagner M, AND Schmitz-Esser S (2015) High diversity of viable bacteria isolates from lymph nodes of slaughtered pigs and its possible impacts for food safety. J. Appl. Microbiol. 119: 1420–1432. doi: 10.1111/jam.12933. |
| [81] | Chaves BD, Ruiz H, Garcia LG, Echeverry A, Thompson L, Miller MF and Brashears MM (2017) High prevalence of Salmonella in lymph nodes and tonsils of swine presented for slaughter in Mexico. Food Prot. Trends 37: 25–28. |
| [82] | Castagna SMF, Schwarz P, Canal CW and Cardoso M (2004) Presence of Salmonella in the intestinal tract and tonsils/mandibular lymph nodes in pigs at slaughter. Arq. Bras. Med. Vet. Zootec. 56: 300–306. (In Portuguese) doi: 10.1590/S0102-09352004000300003. |
| [83] | Gahan CG, O’Driscoll B and Hill C (1996) Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Appl. Environ. Microbiol. 62: 3128–3132. doi: 10.1128/AEM.62.9.3128-3132.1996. |
| [84] | Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF and Foster JW (1999) Control of acid resistance in Escherichia coli. J. Bacteriol. 181: 3525–3535. PMCID: PMC93821, PMID: 10348866. |
| [85] | Varsaki A, Murphy C, Barczynska A, Jordan K and Carroll C (2015) The acid adaptive tolerance response in Campylobacter jejuni induces a global response, as suggested by proteomics and microarrays. Microb. Biotechnol. 8: 974–988. doi: 10.1111/1751-7915.12302. |
| [86] | Smittle RB (2000) Microbiological safety of mayonnaise, salad dressings, and sauces produced in the United States: A review. J. Food Prot. 63: 1144–1153. doi: 10.4315/0362-028X-63.8.1144. |
| [87] | McKellar RC and Knight KP (1999) Growth and survival of various strains of enterohemorrhagic Escherichia coli in hydrochloric and acetic acid. J. Food Prot. 62: 1466–1469. doi: 10.4315/0362-028x-62.12.1466. |
| [88] | Blocker JC and Busta FF (1981) Antimicrobial activity of sorbate. J. Food Protect. 44: 614–622. doi: 10.4315/ 0362-028X-44.8.614. |
| [89] | Hirshfield IN, Terzulli S and O’Byrne C (2003) Weak organic acids: A panoply of effects on bacteria. Sci. Prog. 86: 245–269. doi: 10.3184/003685003783238626. |
| [90] | Aryal S (2020) Biochemical test of Staphylococcus aureus. Available at: https://microbenotes.com/biochemical-test-of-staphylococcus-aureus/ (Accessed on: 20 August 2020). |
| [91] | Bayliss BG and Hall ER (1965) Plasma coagulation by organisms other than Staphylococcus aureus. J. Bacteriol. 89: 101–105. PMID: 14255647; PMCID: PMC315554. |
| [92] | Hammer ND and Skaar EP (2011) Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu. Rev. Microbiol. 65: 129–147. doi: 10.1146/annurev-micro-090110-102851. |
| [93] | Kobylarz MJ, Grigg JC, Sheldon JR, Heinrichs DE and Murphy MEP (2014) SbnG, a citrate synthase in Staphylococcus aureus: A new fold on an old enzyme. J. Biol. Chem. 289: 33797–33807. doi: 10.1074/jbc.M114.603175; PMCID: PMC4256314. |
| [94] | Sheldon JR, Marolda CL and Heinrichs DE (2014) TCA cycle activity in Staphylococcus aureus is essential for iron-regulated syntheses of staphyloferrin A, but not staphyloferrin B: The benefit of a second citrate synthase. Mol. Microbiol. 92: 824–839. doi: 10.1111/mmi.12593. |
| [95] | Beasley FC, Vinés ED, Grigg JC, Zheng Q, Liu S, Lajoie GA, Murphy MEP and Heinrichs DE (2009) Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol. Microbiol. 72: 947–963. doi: 10.1111/j.1365-2958.2009.06698.x. |
| [96] | Cotton JL, Tao J and Balibar CJ (2009) Identification and characterization of the Staphylococcus aureus gene cluster coding for staphyloferrin A. Biochemistry 48: 1025–1035. doi: 10.1021/bi801844c. |
| [97] | Cheung J, Beasley FC, Liu S, Lajoie GA and Heinrichs DE (2009) Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol. Microbiol. 74: 594–608. doi: 10.1111/j.1365-2958.2009.06880.x. |
| [98] | Fuller JR, Vitko NP, Perkowski EF, Scott E, Khatri D, Spontak JS, Thurlow LR and Richardson AR (2011) Identification of a lactate-quinone oxidoreductase in Staphylococcus aureus that is essential for virulence. Front. Cell. Infect. Microbiol. 1: 19. doi: 10.3389/fcimb.2011.00019. |
| [99] | Ferreira MT, Manso AS, Gaspar P, Pinho MG and Neves AR (2013) Effect of oxygen on glucose metabolism: Utilization of lactate in Staphylococcus aureus as revealed by in vivo NMR studies. PLoS ONE 8: e58277. doi: 10.1371/journal.pone. 0058277. |
| [100] | Hara T, Matsui H and Shimizu H (2014) Suppression of microbial metabolic pathways inhibits the generation of the human body odor component diacetyl by Staphylococcus spp. PLoS ONE 9: e111833. doi: 10:1371/ journal.pone.0111833. |
| [101] | Jiang T, Gao C, Ma C and Xu P (2014) Microbial lactate utilization: Enzymes, pathogenesis, and regulation. Trends Microbiol. 22: 589–599. doi: 10.1016/j.tim.2014.05.008. |
| [102] | Bornemeier V, Peters D and Albrecht JA (1997) Effect of added citric acid and acetic acid on the growth of Staphylococcus and Listeria in mayonnaise-based salad. J. Am. Dietet. Assoc. 97 (Suppl.): A-83. doi: 10.1016/S0002-8223(97)00610-X. |
| [103] | Musyoka JN, Abong GO, Mbogo DM, Fuchs R, Low J, Heck S and Muzhingi T (2018) Effects of acidification and preservatives on microbial growth during storage of orange fleshed sweet potato puree. Int. J. Food Sci. 8410747. https://doi.org/10.1155/2018/8410747. |
| [104] | Thool, V. U.; Wadher, B. J.; Bhoosereddy, G. L. Citric acid: A prospective permeabilizer for treatment of VISA infections. Int. J. Curr. Microbiol. Ap. Sci. 2014, 3, 177–183. https://www.ijcmas.com/vol-3-9/V.%20U.Thool,%20et%20al.pdf. |
| [105] | Foster, T. J. Immune evasion by staphylococci. Nat. Rev. Microbiol. 2005, 3, 948–958. doi: 10.1038/nrmicro1289. |
| [106] | DeGroote, M. A.; Fang, F. C. Antimicrobial properties of nitric oxide. In Nitric Oxide and Infection, Vol. 1, Fang, F. C., Ed.; Springer; Boston, MA, USA, 1999; pp. 231–247. doi: 10.1007/0-306-46816-6_12. |
| [107] | Richardson, A. R.; Libby, S. J.; Fang, F. C. A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 2008, 319 (5870), 1672–1676. doi: 10.1126/science. 1155207. |
| [108] | Sakharov DA, Shkurnifov MU, Vagin M Yu, Yashina EI, Karyakin AA and Tonevitsky AG (2010) Relationship between lactate concentrations in active muscle sweat and whole blood. Bull. Exp. Biol. Med. 150: 83–85. doi: 10.1007/s10517-010-1075-0. |
| [109] | Stierna P, Söderlund K and Hultman E (1991) Chronic maxillary sinusitis. Energy metabolism in sinus mucosa and secretion. Acta Otolaryngol. 111: 135–143. doi: 10.3109/ 00016489109137364. |
| [110] | Westrin KM, Stierna P, Söderlund K and Carlsöö B (1992) Lactic acid isomers and fatty acids in sinus secretion: A longitudinal study of bacterial and leukocyte metabolism in experimental sinusitis. Scand. J. Infect. Dis. 24: 765–772. doi: 10.3109/00365549209062462. |
| [111] | Silversides JA, Lappin E and Ferguson AJ (2010) Staphylococcal toxic shock syndrome: Mechanisms and management. Curr. Infect. Dis. Rep. 12: 392–400. doi: 10.1007/s11908-010-0119-y. |
| [112] | Schlebusch S, Schooneveldt JM, Huygens F and Nimmo GR (2009) Prevalence of Staphylococcus aurous strains in an Australian cohort, 1989–2003: Evidence for the low prevalence of the toxic shock toxin and Panton-Valentine leucocidin genes. Eur. J. Clin. Microbiol. Infect. Dis. 28: 1183–1189. doi: 10.1007/s10096-009-0761-1. |
| [113] | Charlier C, Cretenet M, Even S and Le Loir Y (2009) Interactins between Staphylococcus aureus and lactic acid bacteria: An old story with new perspectives. Int. J. Food Microbiol. 131: 30–39. doi: 10.1016/j.ijfoodmicro.2008.06. 032. |
| [114] | Reid G and Bruce AW (2003) Urogenital infections in women: Can probiotics help? Postgrad. Med. J. 79: 428–432. doi: 10.1136/pmj.79.934.428. |
APA Style
Ross Carlton Beier, Kathleen Andrews, Toni Lee Poole, Roger Bruce Harvey, Tawni Lyn Crippen, et al. (2020). Interactions of Organic Acids with Staphylococcus aureus and MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Feces. International Journal of Microbiology and Biotechnology, 5(4), 165-183. https://doi.org/10.11648/j.ijmb.20200504.12
ACS Style
Ross Carlton Beier; Kathleen Andrews; Toni Lee Poole; Roger Bruce Harvey; Tawni Lyn Crippen, et al. Interactions of Organic Acids with Staphylococcus aureus and MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Feces. Int. J. Microbiol. Biotechnol. 2020, 5(4), 165-183. doi: 10.11648/j.ijmb.20200504.12
AMA Style
Ross Carlton Beier, Kathleen Andrews, Toni Lee Poole, Roger Bruce Harvey, Tawni Lyn Crippen, et al. Interactions of Organic Acids with Staphylococcus aureus and MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Feces. Int J Microbiol Biotechnol. 2020;5(4):165-183. doi: 10.11648/j.ijmb.20200504.12
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Download@article{10.11648/j.ijmb.20200504.12,
author = {Ross Carlton Beier and Kathleen Andrews and Toni Lee Poole and Roger Bruce Harvey and Tawni Lyn Crippen and Robin Carl Anderson and David James Nisbet},
title = {Interactions of Organic Acids with Staphylococcus aureus and MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Feces},
journal = {International Journal of Microbiology and Biotechnology},
volume = {5},
number = {4},
pages = {165-183},
doi = {10.11648/j.ijmb.20200504.12},
url = {https://doi.org/10.11648/j.ijmb.20200504.12},
eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ijmb.20200504.12},
abstract = {Staphylococcus aureus is a Gram-positive bacterium affecting human health, and a major cause of skin infections, endocarditis, meningitis, and sepsis. Methicillin-resistant S. aureus (MRSA) is a worldwide health concern, occurs in food animals, is consistently found in swine, and improved strategies are needed to ensure the removal of MRSA from food products. A total of 164 S. aureus strains were isolated from swine mandibular lymph node tissue, commercial pork sausage meat, and feces. These strains were tested for methicillin-resistance, and 7 of the strains isolated from the mandibular lymph node tissue and pork sausage meat were resistant to cefoxitin and oxacillin, and tested positive for staph specific rRNA and for the mecA gene and are therefore, MRSA strains. An intracellular MRSA contamination of 8.2% within swine lymph node tissue and 5.8% MRSA contamination in pork sausage meat was demonstrated. Lymph node tissue may be utilized in producing pork sausage; therefore, the prevalence of MRSA in final pork products may not only be caused by surface contamination, but by internal tissue infection. The strains were tested for susceptibility to six organic acids (OAs) citric, L-lactic, butyric, acetic, propionic, and formic acid. The pH was determined at each of the minimum inhibitory concentrations (MICs) observed for the S. aureus strains. The Henderson-Hasselbalch equation was used to calculate the ratio of the undissociated to dissociated OA concentrations, and the molar concentrations of each were calculated from the total OA present and the ratio. Inhibition of S. aureus did not correlate with pH or the undissociated OA concentrations, but it did correlate with the dissociated OA concentrations. A dissociated OA concentration of 21 mM was successful for inhibiting the S. aureus strains tested. Studies must be conducted in vivo to confirm this concentration value. Acetic, butyric, formic, and propionic acid were the most effective OAs tested against S. aureus.},
year = {2020}
}
TY - JOUR T1 - Interactions of Organic Acids with Staphylococcus aureus and MRSA Strains from Swine Mandibular Lymph Node Tissue, Commercial Pork Sausage Meat and Feces AU - Ross Carlton Beier AU - Kathleen Andrews AU - Toni Lee Poole AU - Roger Bruce Harvey AU - Tawni Lyn Crippen AU - Robin Carl Anderson AU - David James Nisbet Y1 - 2020/11/19 PY - 2020 N1 - https://doi.org/10.11648/j.ijmb.20200504.12 DO - 10.11648/j.ijmb.20200504.12 T2 - International Journal of Microbiology and Biotechnology JF - International Journal of Microbiology and Biotechnology JO - International Journal of Microbiology and Biotechnology SP - 165 EP - 183 PB - Science Publishing Group SN - 2578-9686 UR - https://doi.org/10.11648/j.ijmb.20200504.12 AB - Staphylococcus aureus is a Gram-positive bacterium affecting human health, and a major cause of skin infections, endocarditis, meningitis, and sepsis. Methicillin-resistant S. aureus (MRSA) is a worldwide health concern, occurs in food animals, is consistently found in swine, and improved strategies are needed to ensure the removal of MRSA from food products. A total of 164 S. aureus strains were isolated from swine mandibular lymph node tissue, commercial pork sausage meat, and feces. These strains were tested for methicillin-resistance, and 7 of the strains isolated from the mandibular lymph node tissue and pork sausage meat were resistant to cefoxitin and oxacillin, and tested positive for staph specific rRNA and for the mecA gene and are therefore, MRSA strains. An intracellular MRSA contamination of 8.2% within swine lymph node tissue and 5.8% MRSA contamination in pork sausage meat was demonstrated. Lymph node tissue may be utilized in producing pork sausage; therefore, the prevalence of MRSA in final pork products may not only be caused by surface contamination, but by internal tissue infection. The strains were tested for susceptibility to six organic acids (OAs) citric, L-lactic, butyric, acetic, propionic, and formic acid. The pH was determined at each of the minimum inhibitory concentrations (MICs) observed for the S. aureus strains. The Henderson-Hasselbalch equation was used to calculate the ratio of the undissociated to dissociated OA concentrations, and the molar concentrations of each were calculated from the total OA present and the ratio. Inhibition of S. aureus did not correlate with pH or the undissociated OA concentrations, but it did correlate with the dissociated OA concentrations. A dissociated OA concentration of 21 mM was successful for inhibiting the S. aureus strains tested. Studies must be conducted in vivo to confirm this concentration value. Acetic, butyric, formic, and propionic acid were the most effective OAs tested against S. aureus. VL - 5 IS - 4 ER -
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