Epidemiology, Pathogenicity, Animal Infections, Antibiotic Resistance, Public Health Significance, and Economic Impact of Staphylococcus Aureus: A Comprehensive Review

Mahendra Pal¹, Gemechu Berhanu Kerorsa², Lencho Megersa Marami³ and Venkataramana Kandi^4,

¹Narayan Consultancy on Veterinary Public Health and Microbiology, Anand, Gujarat, India

²College of Agriculture and Veterinary Medicine, Dambi Dollo University, Dambi Dollo, Ethiopia

³College of Agriculture and Veterinary Science, Ambo University, Ambo Ethiopia

⁴Department of Microbiology, Prathima Institute of Medical Sciences, Karimnagar, Telangana, India

Cite this paper

Mahendra Pal, Gemechu Berhanu Kerorsa, Lencho Megersa Marami and Venkataramana Kandi. Epidemiology, Pathogenicity, Animal Infections, Antibiotic Resistance, Public Health Significance, and Economic Impact of Staphylococcus Aureus: A Comprehensive Review. American Journal of Public Health Research. 2020; 8(1):14-21. doi: 10.12691/AJPHR-8-1-3

Abstract

Staphylococcus aureus (S. aureus) is a gram-positive bacterium that has a greater impact on animal and human health by causing various diseases. S. aureus is present as normal flora of the skin and mucous membranes of both humans and animals but can cause disease when it gets the chance to invade either due to trauma or because of impaired immune responses of the host. Different virulence factors are involved in the mechanisms of pathogenesis of S. aureus which include surface proteins, enzymes, toxins, and others. These virulence factors play an important role in invasion, colonization, and survival of S. aureus in the host to cause staphylococcal diseases. Infections of S. aureus pose a major public health threat owing to its ability to cause mild to severe/life-threatening human diseases. Methicillin-resistant S. aureus (MRSA) has become a pathogen of increasing importance in hospitals (nosocomial infection) and the community. It can be mainly transmitted to humans by the consumption of food of animal origin. Foods associated with outbreaks of staphylococcal food poisoning include meat and meat products, poultry, and egg products, milk and dairy products, salads, cream-filled bakery products, and sandwich fillings. Additionally, it has great economic importance as it causes different diseases in animals. MRSA shows resistance to different antibiotics including penicillin, methicillin, vancomycin, and others owing to the presence of different antibiotic resistance genes and other resistance mechanisms.

Keywords

Staphylococcus aureus, virulence factors, methicillin resistant Staphylococcus aureus, vancomycin, animals, public health, antibiotic resistance genes, nosocomial infection, food of animal origin

Copyright

This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

References

[1]	Akanbi, O.E., Njom, H.A., Fri, J., Otigbu, A.C. and Clarke, A.M. (2017). Antimicrobial Susceptibility of Staphylococcus aureus Isolated from Recreational Waters and Beach Sand in Eastern Cape Province of South Africa. International Journal of Environmental Research and Public Health, 14: 1001.
[2]	Quinn, P.J., Markey, B.K., Leonard, F.C., FitzPatrick, E.S., Fanning, S. and Hartigan, P.J. (2011). Staphylococcus Species: Veterinary Microbiology and Microbial Disease. 2nd Edition. Dublin. Pp. 159-165.
[3]	Pal. M. 2001. Epidemiology of staphylococcal food poisoning. Beverage and Food World 28: 11-13.
[4]	Butaye, P., Struelens, M. and Uyehera, L. (2007). MRSA, report on zoonotic agent in Belgium. Trend and sources by working group on food born infections and intoxication. Drug Research,20: 59-61.
[5]	Li, Y., Li, X., Huang, T., Xu, K. and Li, C. (2019). Molecular characteristics and virulence gene profiles of Staphylococcus aureus isolates in Hainan, China. BMC Infectious Diseases. 19:873.
[6]	Hachemi, A., Zenia, S., Denia, M.F., Guessoum, M., Hachemi, M.M. and Ait-Oudhia, K. (2019). Epidemiological study of sausage in Algeria: Prevalence, quality assessment, and antibiotic resistance of Staphylococcus aureusisolates and the risk factors associated with consumer habits affecting foodborne poisoning, Veterinary World, 12(8): 1240-1250.
[7]	Normanno, G., La Salandra, G., Dambrosio, A., Quaglia, N., Corrente, M., Parisi, A., et al. (2007). Occurrence, characterization and antimicrobial resistance of enterotoxigenicStaphylococcus aureusisolated from meat and dairy products. International Journal of Food Microbiology, 115(3): 290-296.
[8]	EFSA, (European Food Safety Authority) (2009). Assessment of the Public Health significance of methicillin resistant Staphylococcus aureus (MRSA) in animals and foods. Scientific opinion of the panel on biological hazards. The EFSA Journal,993: 1-73.
[9]	Pal, M. 2007. Zoonoses. 2nd Edition. Satyam Publishers, Jaipur, India.
[10]	Deyno, S., Toma, A., Worku, M. and Bekele, M. (2017). Antimicrobial resistance profile of Staphylococcus aureus isolates isolated from ear discharges of patients at University of Hawassa comprehensive specialized hospital. BMC Pharmacology and Toxicology, 18:35.
[11]	Liu, B., Sun, H., Pan, Y., Zhai, Y., Cai, T. and Yuan, X. (2018). Prevalence, resistance pattern, and molecular characterization of Staphylococcus aureusisolates from healthy animals and sick populations in Henan Province, China. Gut Pathogens, 10:31.
[12]	Stewart, C.M. (2003). Staphylococcus aureus and Staphylococcal Enterotoxins. In: Hocking AD (ed) Food borne Microorganisms of Public Health Significance. 6th ed. Australian Institute of Food Science and Technology (NSW Branch), Sydney, Pp. 359-380.
[13]	Jaggi, P., Paule, S.M., Peterson, L.R. and Tan, T.Q. (2007). Characteristics of Staphylococcus aureus Infections, Chicago Pediatric Hospital. Emerging Infectious Diseases, 13(2): 311-314.
[14]	Ramana KV, Mohanty SK, Wilson CG. Staphylococcus aureus colonization of anterior nares of school going children. Indian J Pediatr. 2009; 76(8):813-6.
[15]	Ramana KV, Mohanty SK, Kumar A. In-vitro activities of current antimicrobial agents against isolates of pyoderma. Indian J Dermatol Venereol Leprol 2008; 74:430
[16]	Pollitt, E.J.G., Szkuta, P.T., Burns, N. and Foster, S.J. (2018). Staphylococcus aureusinfection dynamics. PLoS Pathogens, 14(6): e1007112.
[17]	Dini, M., Shokoohizadeh, L., Jalilian, F.A., Moradi, A. and Arabestani, M.R. (2019). Genotyping and characterization of prophage patterns in clinical isolates ofStaphylococcus aureus. BMC Research Notes, 12:669.
[18]	Wang, X., Liu, Q., Zhang, H., Li, X., Huang, W., Fu, Q. et al. (2018). Molecular Characteristics of Community-Associated Staphylococcus aureus Isolates from Pediatric Patients with Bloodstream Infections Between 2012 and 2017 in Shanghai, China. Frontiers in Microbiology, 9:1211.
[19]	Chambers, H.F. and Deleo, F.R. (2009). Waves of Resistance: Staphylococcus aureus in the Antibiotic Era. Nature Reviews Microbiology, 7: 629-641.
[20]	Schwalm, N., Verghese, B. and Knabel, S. (2011): A novel multiplex PCR method for detecting the major clonal complexes of MRSA in nasal isolates from a Pennsylvania hospital. Journal of Microbiological Methods,86: 379-382.
[21]	Aung, M.S., San, T., Urushibara, N., San, N., Oo, W.M., Soe, P.E., et al. (2019). Molecular Characterization of Methicillin-Susceptible and Resistant Staphylococcus aureus Harboring Panton Valentine Leukocidin-Encoding Bacteriophages in a Tertiary Care Hospital in Myanmar. Microbial Drug Resistance, 10:1-8.
[22]	Hasman, H., Moodley, A., Guardabassi, L., Stegger, M., Skov, R. and Aarestrup, F. (2010). Spa type distribution in Staphylococcus aureusoriginating from pigs, cattle and poultry. Veterinary Microbiology, 141(3): 326-331.
[23]	Cuny, C., Friedrich, A., Kozytska, S., Layer, F., Nübel, U., Ohlsen, K., et al. (2010). Emergence of MRSA in different animal species. International Journal of Medical Microbiology, 300(2): 109-117.
[24]	Nemati, M., Hermans, K., Lipinska, U., Denis, O., Deplano, A., Struelens, M., Pasmans, F. and Haesebrouck, F. (2008). Antimicrobial resistance of Staphylococcus aureus isolates from poultry. First detection of livestock associated methicillin resistant strain ST398. Antimicrobial Agents and Chemotherapy, 52(10): 3817-3819.
[25]	Grave, K., Torren-Edo, J. and Mackay, D. (2010). Comparison of the sales of veterinary antibacterial agents between 10 European countries. Journal of Antimicrobial Chemotherapy, 65(9): 2037-2040.
[26]	Ayele, Y., Gutema, F.D., Edao, B.M., Girma, R., Tufa, T.B., Beyene, T.J., et al. (2017). Assessment of Staphylococcus aureus along milk value chain and its public health importance in Sebeta, central Oromia, Ethiopia. BMC Microbiology, 17: 141.
[27]	John, J., George, S., Nori, S.R.C. and Nelson-Sathi, S. (2019). Phylogenomic Analysis Reveals the Evolutionary Route of Resistant Genes in Staphylococcus aureus. Genome Biol. Evol. 11(10): 2917-2926.
[28]	Catry, B., Van Duijkeren, E., Pomba, M., Greko, C., Moreno, M., Pyorala, S., Ruzauskas, M., et al. (2010). Reflection paper on MRSA in food-producing and companion animals. Epidemiology and control options for human and animal health. Epidemiology and Infection, 138(5): 626-644.
[29]	Kandi V. Coral Dermatitis or Infectious Dermatitis: Report of a Case of Staphylococcus Aureus Infection of Skin After Scuba Diving. Cureus 2018; 10(2): e2196.
[30]	Van Belkum, A., Melles, D., Nouwen, J., van Leeuwen, W., Van Wamel, W., Wertheim, H., et al. (2009). Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infectious, Genetetic and Evolution, 9(1): 32-47.
[31]	Lowy, F. D, (2003): Antimicrobial resistance, the example of Staphylococcus aureus. The Journal of Clinical Investigation, 111(9): 1265-1273.
[32]	Chakravarty, S. and Massé, E. (2019). RNA-dependent regulation of virulence in pathogenic bacteria. Frontiers in Cellular and Infection Microbiology, 9:337.
[33]	Foster, T.J. (2005). Immune evasion by Staphylococci. Nature Reviews Microbiology, 3: 948-958.
[34]	Kong, C., Neoh, H. and Nathan, S. (2016). Targeting Staphylococcus aureus Toxins: A Potential form of Anti-Virulence Therapy. Toxins, 8:72.
[35]	Kashif, A., McClure, J.A., Lakhundi, S., Pham, M., Chen, S., Conly, J.M. and Zhang, K. (2019). Staphylococcus aureus ST398 Virulence is Associated with Factors Carried on Prophage ᶲSa3. Frontiers in Microbiology, 10: 2219.
[36]	Clauditz, A., Resch, A., Wieland, K., Peschel, A. And Götz, F. (2006). Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infection and Immunity, 74(8): 4950-4953.
[37]	Yilmaz, E.S. and Aslantas, O. (2017). Antimicrobial resistance and underlying mechanisms in Staphylococcus aureus isolates. Asian Pacific Journal of Tropical Medicine, 10(11): 1059-1064.
[38]	Weidenmaier, C., Kokaikun, J. and Kristian, S. (2004). Role of teichoic acids in Staphylococcus aureusnasal colonization, a major risk factor in nosocomial infections. Nature Medicine, 10(3): 243-245.
[39]	Otto, M. (2004): Quorum sensing control in staphylococci a target for antimicrobial drug therapy. FEMS Microbiology Letters, 241(2): 135-41.
[40]	Haas, P., De Haas, C. and Kleibeuker, W. (2004). N-terminal residues of the chemotaxis inhibitory protein of Staphylococcus aureusare essential for blocking formylated peptide receptor but not C5a receptor. Journal of Immunology, 173(9): 5704-5711.
[41]	Otto, M. (2008). Staphylococcal Biofilms. Current Topics in Microbiology and Immunology, 322: 207-228.
[42]	Patel, R. (2005). Biofilms and antimicrobial resistance. Clinical Orthopedics and Related Research, 5: 41-47.
[43]	Fotou, K., Tzora, A., Voidarou, C., Alexopoulos, A., Plessas, S., Avgeris, I., Bezirtzoglou, E., Akrida-Demertzi, K. and Demertzis, P. (2011). Isolation of microbial pathogens of subclinical mastitis from raw sheep’s milk of Epirus (Greece) and their role in its hygiene. Anaerobe, 17(6): 315-319.
[44]	Pal, M. 2018. Mastitis: A major production disease of dairy animals. Agriculture World 4: 46-51.
[45]	Kalsoom, F., Syed, N. and Farzana, J. (2004). Antibiotic resistance pattern against various isolates of Staphylococcus aureus from raw milk samples. Journal of Research Science, 15(2): 145-151.
[46]	Voss, A., Loeffen, F., Bakker, J., Klaassen, C. and Wulf, M. (2005). Methicillin resistant Staphylococcus aureus in pig farming. Emerging Infectious Disease, 11(12): 1965-1966.
[47]	Persoons, D., Hoorebeke, S.V., Hermans, K., Butaye, P., Kruif, A., Haesebrouck, F., et al., (2009). Methicillin-Resistant Staphylococcus aureus in Poultry. Emerging Infectious Diseases, 15(3): 452-453.
[48]	Pal, M. (1992). An epidemic of systemic staphylococcosis in White Leghorn chicks. Veterinary Review 7: 24-25.
[49]	Saif, M. (2003): Disease of Poultry. 11th ed., Lowa State University Press, Pp. 1134-1144.
[50]	Kwoji, I.D., Tambuwal, F.M., Abubakar, M.B., Yakubu, Y., Bitrus, A.A. and Jauro, S. (2017). Occurrence of methicillin resistant Staphylococcus aureusin chickens and farm personnel in Sokoto, North-western Nigeria. Journal of Advanced Veterinary and Animal Research, 4(3): 255-260.
[51]	Hanning, I., Gilmore, D., Pendleton, S., Fleck, S., Clement, A. and Park, S.H. (2012). Characterization of Staphylococcus aureus Isolates from Retail Chicken Carcasses and Pet Workers in Northwest Arkansas. Journal of Food Protection, 75(1): 174-178
[52]	Arfatahery, N., Mirshafiey, A., Abedimohtasab, T.P. and Zeinolabedinizamani, M. (2015). Study of the prevalence of Staphylococcus aureusin marine and farmed shrimps in Iran aiming the future development of a prophylactic vaccine. Procedia in Vaccinology, 9:44-49.
[53]	Bujjamma, P. and Padmavathi, P. (2015). Prevalence of Staphylococcus aureusin Fish Samples of Local Domestic Fish Market. International Journal of Current Microbiology and Applied Sciences, 4(5):427-433.
[54]	Donham, K.J. (2010). Community and occupational health concerns in pork production. Journal of Animal Science, 88: 102-111.
[55]	Klare, I., Konstabel, C., Badstübner, D., Werner, G. and Witte, W. (2003). Occurrence and spread of antibiotic resistances in E. faecium. International Journal of Food Microbiology, 88(2): 269-290.
[56]	Wassmann, C.S., Lund, L.C., Thorsing, M., Lauritzen, S.P., Kolmos, H.J., Kallipolitis, B.H., et al. (2018). Molecular mechanisms of thioridazine resistance in Staphylococcus aureus. PLoS ONE, 13(8): e0201767.
[57]	Wang, H., Liu, Y., Du, N., Shen, E., Chen, H., Niu, J., et al. (2009). Molecular Evidence for Spread of Two Major Methicillin-Resistant Staphylococcus aureusClones with a Unique Geographic Distribution in Chinese Hospitals. Antimicrobial Agents and Chemotherapy, 53(2): 512-518.
[58]	Osman, K., Badr, J., Al-Maary, K.S., Moussa, I.M., Hessain, A.M., Girah Z.M., et al. (2016). Prevalence of the Antibiotic Resistance Genes in Coagulase-Positive-and Negative-Staphylococcus in Chicken Meat Retailed to Consumers. Frontiers in Microbiology, 7: 1846.
[59]	Li, S.M., Zhou, Y.F., Li, L., Fang, L.X., Duan, J.H., Liu, F.R., et al. (2018). Characterization of the Multi-Drug Resistance Gene cfr in Methicillin-Resistant Staphylococcus aureus (MRSA) Strains Isolated from Animals and Humans in China. Frontiers in Microbiology, 9: 2925.
[60]	Otarigho, B. and Falade, M.O. (2018). Analysis of antibiotics resistant genes in different strains of Staphylococcus aureus. Bioinformation, 14(3):113-122.
[61]	Abdolmaleki, Z., Mashak, Z. and Dehkordi, F.S. (2019). Phenotypic and genotypic characterization of antibiotic resistance in the methicillin resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrobial Resistance and Infection Control, 8:54
[62]	Nworie, A., Madubuko, E.F. and Eze, U.A. (2013). Nasal carriage of methicillin-Resistant Staphylococcus aureusamongst meat sellers in Abakaliki Metropolis, Ebonyi State, Nigeria. Microbiology Research International, 2013; 1(3):48-53.
[63]	Ramana KV and Rao R. Significance of Screening for Colonization and Vancomycin Resistance in Staphylococcus aureus Isolated from Anterior Nares of School Going Children. Online J Health Allied Scs. 2009; 8(3):20.
[64]	McCallum, N., Berger-Bächi, B. and Senn, M. (2010): Regulation of antibiotic resistance in Staphylococcus aureus. International Journal of Medical Microbiology, 300(1): 118-129.
[65]	Périchon, B. and Courvalin, P. (2009). VanA type vancomycin resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 53(11): 4580-4587.
[66]	Udou, T. (2004). Dissemination of nosocomial multiple aminoglycoside resistant Staphylococcus aureuscaused by horizontal transfer of the resistance determinant (aacA/aphD) and clonal spread of resistant strains. AJIC, 32: 215-219.
[67]	Lina, G., Quaglia, A., Reverdy, M., Leclercq, R., Vandenesch, F. and Etienne, J. (1999). Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramin among Staphylococci. Antimicrobial Agents and Chemotherapy, 43(5): 1062-1066.
[68]	Mišic´, M,C., Ukic´, J., Vidanovic´, D., Šekler, M., Matic´, S., Vukašinovic´, M. et al. (2017) Prevalence of Genotypes That Determine Resistance of Staphylococci to Macrolides and Lincosamides in Serbia. Frontiers in Public Health, 5: 200.
[69]	Argudin, M.A., Mendoza, M.C. and Rodico, M.R. (2010). Food poisoning and S. aureusenterotoxins. Toxins, 2(7): 1751-1773.
[70]	FDA, (2012). Bad bug book, Foodborne Pathogenic Microorganisms and Natural Toxins Handbook. 2nd ed. US Food and Drug Administration, Silver Spring, Pp. 87-92.
[71]	Akpaka, P.E., Robertsa, R. and Moneckeb, S. (2017). Molecular characterization of antimicrobial resistance genes against Staphylococcus aureusisolates from Trinidad and Tobago. Journal of Infection and Public Health, 10: 316-323.
[72]	Awale, M., Dudhatra, G., Avinash, K., Chauhan, B., Kamani, D., Modi, C., et al. (2012). Bovine mastitis, a threat to economy. Open Access Scientific Reports, 1: 295.
[73]	Halasa, T., Nielen, M., De Roos, A., Van Hoorne, R., De Jong, G., Lam, T., Van Werven, T. and Hogeveen, H. (2009). Production loss due to new subclinical mastitis in Dutch dairy cows estimated with a test day model. Journal of Dairy Science, 92(2): 599-606.