User:Hayley.bowling/Staphylococcus hyicus

Staphylococcus hyicus
Scientific classification
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Species:
S. hyicus
Binomial name
Staphylococcus hyicus
Sompolinsky 1953; Devriese et al. 1978

Staphylococcus hyicus is a Gram-positive, facultatively anaerobic bacterium in the genus Staphylococcus. It consists of clustered cocci and forms white circular colonies when grown on blood agar.[1] S. hyicus is a known animal pathogen causing skin disease in cattle,[2] horses,[3] and pigs.[4] Most notably, it is the causative agent of exudative epidermitis, also known as greasy pig disease, in piglets.[5] The condition is caused by exfoliative toxins that S. hyicus that disrupt desmosomal junctions thus allowing for invasion.[6] S. hyicus is generally considered non-zoonotic[1]; however it has been shown to cause bacteremia and sepsis in humans.[7][8]

With its global distribution S. hyicus commonly infects pig herds worldwide.[1] It can be found on asymptomatic carrier pigs at sites such as the skin, mucosa of nasal cavity, conjunctiva, and genitals (vagina of sow and prepuce of boar).[1][9] It can be devastating to a pig farmer's livelihood and is often a concern because it shows increasing resistance to many antibiotics.[10]

Infection with S. hyicus can be prevented with an autogenous vaccine.[11] Managing the pigs can prevent disease and reduce the severity of an outbreak.[12] Treatment includes topical sprays and oils[13] as well as antibiotics which should be tested to ensure S. hyicus susceptibility.[14][15][13]

Gram positive cocci in clusters. This could be S. hyicus but it is impossible to tell without further diagnostics.

Microbiology

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History and Taxonomy

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The first known description of exudative epidermitis in pigs was in 1842 and the causative agent was later identified as Micrococcus hyicus in 1953.[1][16] Based on phenotypic similarities, M. hyicus was moved to the Staphylococcus genus in 1965.[1][17] The similar bacterium Staphylococcus chromogenes was considered a subspecies of S. hyicus until it was elevated to its own species in 1986.[16][18] Other bacteria closely related to S. hyicus include S. schleiferi, S. intermedius, S. pseudintermedius, and S. felis.[19]

Morphological Characteristics

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Staphylococus hyicus, like other members of the Staphylococcus genus, is a gram-positive coccus that forms clusters.[1][20] It is facultatively anaerobic.[19] Six different serotypes have been identified to date.[20] The bacterium is quite resistant and can remain viable in the environment for long periods of time without drying out.[20][9]

On blood agar, S. hyicus colonies are medium in size (1 to 3 mm in diameter) and appear white, opaque, convex, and circular.[1][21][19] Rarely, some have been observed to appear yellow on sheep blood agar but the vast majories of colonies do not produce any pigment.[22] S. hyicus colonies normally do not show hemolysis on blood agar however they do show a characteristic small zone of hemolysis on chocolate agar.[21]

Biochemistry and Identification

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The identification of S. hyicus and differentiation from similar organisms may require extensive biochemical testing.[21] Most strains of S. hyicus are coagulase positive; however, some strains isolated from both pigs and cattle have been found to be coagulase negative so it can be considered coagulase variable.[1][21][23][7] This variability can make it difficult to tell apart from similar bacteria such as Staphlococcus agnetis without PCR based methods or genotyping.[21][23] S. hyicus is catalase positive and oxidase negative.[1][21][19] It also normally shows DNase activity.[21][22]

S. hyicus produces a bacteriolytic enzyme and an S. hyicus-specific teichoic acid.[21] Porcine strains express surface receptors for immunoglobulin G but these are not commonly expressed by bovine strains.[21] Most strains are capable of fermentation of glucose, fructose, mannose, lactose, and trehalose but not maltose.[19][21]

Differentiation of S. hyicus from other members of the genus can be done based on the sequence of its 16S rRNA gene[22][24][25] or thermonuclease (nuc) gene[26]. The complete genome (2,472,129 base pairs) of S. hyicus ATCC 11249T was also sequenced and annotated in 2015.[27]

Virulence and Resistance

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Virulence

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Division of S. hyicus into virulent and avirulent strains is based on the production of an exfoliative toxin (virulence factor), which produces the clinical presentation of exudative epidermitis, as these toxins specifically target the stratum granulosum and stratum spinosum.[1][5][28] S. hyicus exfoliative toxin (SHET) producing strains are further divided into plasmid carrying (SHETB) and plasmidless (SHETA).[29][30] It was found that genes encoding four different exfoliative toxins (ExhA, ExhB, ExhC and ExhD) were homologous to SHETB.[31] These exotoxins are similar to the exfoliative toxin (ETA, ETB, ETD) that Staphylococcus aureus produces.[1][31][32] The mechanism of action is via serine protease-like exfoliative toxins.[31] Swine desmoglein 1 (Dsg1) is a desmosomal intracellular adhesion molecule that is cleaved by the exfoliative toxins produced by S. hyicus allowing for separation of stratum granulosum and stratum spinosum.[6][1] Other virulence factors have been reported, the production of protein A with binding sites for IgG allows for evasion from phagocytes, coagulase production to form clots, surface fibronectin-binding proteins for adhesion and production of staphylokinase and lipase to evade host defences.[1] These virulence factors in combination with other factors like age, being immunocompromised, genetic susceptibility, trauma (physical, chemical, solar), disease status and environmental conditions can vary the expression of exudative epidermitis experienced.[1]

Resistance

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S. hyicus has frequently been reported to be resistant to a range of antimicrobial agents[33]. S. hyicus has demonstrated resistance to penicillin, streptomycin, tetracycline, trimethoprim, erythromycin, sulfonamides, lincomycin and chloramphenicol.[33] Further resistance testing of S. hyicus isolates found high resistance to penicillin, macrolides, tetracycline, sulfonamides and streptomycin, but S. hyicus was sensitive to ciprofloxacin, chloramphenicol and florfenicol.[10][33] This multi-drug resistance has been linked to certain genes. For beta-lactam resistance, the mechanism is by altering penicillin binding protein production which is encoded by mecA.[33][34]Further, it has been suggested that resistance may be passed between staphylococcal species especially when treating pigs prophylactically.[34] Other implicated plasmid resistance genes are tet(L) for tetracyclines, erm(C) for macrolides, lincosamides and streptogramins and the pS194-like str gene is for chloramphenicol and streptomycin resistance.[33] Genetic elements for resistance to methicillin and zinc have been reported, therefore susceptibility testing is recommended before treatment.[1]

Disease in All Species

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S. hyicus is most noted for causing disease in pigs but has been seen to cause problems in other species as well.

 
A dead piglet, showing some mild characteristic lesions of exudative dermatitis.

Swine

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S. hyicus is the causative agent of exudative dermatitis in piglets. This condition is commonly referred to as greasy pig disease. It gets this nickname from Its classic appearance of scabs all over the body. It presents in piglets nursery age or younger most often, and can lead to death as the piglet loses fluid through the skin and become dehydrated.[35] The morbidity varies greatly but can be up to 80% in some instances. Lesions in the form of macules are usually most severe around the lips, nose, and ears. These lesions are characteristic in their release of oily exudate. As it progresses to the entire body, treatment becomes more difficult.[36] The bacteria can be normally present on the skin, in the nose as well as the vagina and prepuce. For this reason it is considered endemic in most herds, though the pathogenesis may be sporadic. It can also cause bacteremia and sepsis in piglets which if they recover can result in arthritis and poor growth that can affect them for life.[20]

Cattle

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The bacterial species has been isolated from milk in dairy herds and is one of the more uncommon causes of contagious mastitis in the Staphylococcus species.[37] This type of mastitis can be very difficult to control as cows can spread it without being clinically ill. This bacteria most commonly causes persistent intramammary infections, which can lead to the cow needing to be culled from the herd.[38]

Poultry

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S.hyicus has been rarely reported in poultry animals, but is thought to be a cause of bacterial chondro-necrosis along with other species such as Staphlococcus agnetis. Lameness is a cause for concern in the industry and contributes to economic losses as well as welfare issues.[39] It is considered to e a normal part of poultry skin flora and may be a contributor to fowl pox.[40]This bacteria has also been cultured from chicken meat labelled for human consumption, and could be a cause of Staphylococcus food poisoning.[41] In one study the strains of S. hyicus found was resistant to every antibiotic tested. This is concerning because it means these resistant bacteria are in contact with people and could have large health implications if infected.[42]

Horses

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In horses, S. hyicus is not a common pathogen but when it does infect, it affects the skin of the distal limbs. This condition can be referred to as summer eczema or grease heel. It results in scabs and hair loss. It can heal on its own or can be easily treated with antibiotics the bacteria is susceptible to.[43] In this way it is often a cosmetic issue or a slight discomfort, and is not life threatening like in other species. S. hyicus is almost exclusively seen in lesions and is not a normal part of the healthy equine skin flora.[44]

Humans

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Humans being affected by S. hyicus is rare and for this reason is not considered a common zoonosis. There is a higher risk of people being infected if the work in close contact with infected pigs frequently, such as one case reported in a farmer with a previously infected foot causing bacteremia[7]. One notable case is a man who was diagnosed with a case of infectious spondylodiscitis and septicemia. Culture of his infected culture bone and blood was confirmed to have S. hyicus present, suggesting it was the causative agent.[8]This case is concerning because he was considered immunocompetent, which is often not the case for rare bacterial infections. There has been very few human cases found other than these rare instances, and it is not currently considered a risk to human health.[1]

Role of S. hyicus in Exudative Epidermitis (Greasy Pig Disease)

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Epidemiological background:

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Endemic infection with S. hyicus is a common finding worldwide; however the development of exudative epidermitis is based on opportunity and the age of the pigs involved[1][4][5]. Rarely there are exudative epidermitis outbreaks with whole herds affected[20]. However, in cases of outbreak it is often the youngest whom are most severely affected with high mortality and morbidity[4][5][20]. Predilection for the outbreak of disease include newly founded herds, gilt litters, and an overall diminished passive transfer of antibodies for S. hyicus from sow to piglets[20]; and for the individual animal, those that have open wounds, sores or have been exposed to a form of trauma or irritation are predisposed to develop infection of S. hyicus[20]. Additional factors that may increase individual animal susceptibility to S. hyicus-caused exudative epidermitis include parasitism, viral infection, and other immunity issues, nutritional deficiencies, issues with management and hygiene practices, and possible genetic susceptibility[20][5].

Pathogenesis

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Early clinical signs can include anorexia, lethargy, and reddening of skin specifically in the inguinal and axillary regions[20][5].

Epidermal inflammatory processes accompanied by exudate are attributed to exfoliative toxins of S. hyicus[4][45][6]. Exfoliative toxins will cleave swine desmoglein-1 (Dsg1); therefore, creating an opportunity for epidermal bacterial invasion with the splitting of the stratum spinosum and stratum granulosum[6][20]. With bacterial invasion, 1 to 2 cm (diameter) brown lesions will begin to appear within the 24 to 48 hour range; and lesions will first appear cranially before progressing posteriorly as crusting ulcers with possible formation of suppurative folliculitis[5][20]. However, in younger animals that may die within 3 to 5 days, crusting ulcers may only be situated in the cranial region due to lack of time to progress[20]. Often the young piglets severely affected by S. hyicus causing exudative epidermitis die from dehydration characterized by a loss of protein serum and electrolytes[20].

Besides the characteristic brown lesions of the dermis, ulcerative lesions can form in the mucosa of the mouth and on the tongue[5][20]. Additionally, peripheral lymph nodes will swell, and internal organs such as the kidney and lungs may become distended[5][20].

Areas of the Body Affected:

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  • Head, neck, feet, general body, mouth and tongue[5][20]
  • Kidneys and ureters may become distended with mucous and debris collection; additionally lungs may accumulate congestion during the disease process[5]

Diagnosis

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Exudative epidermitis is often fatal in piglets especially those within the 1 to 5 week-old range as they are most at risk for the development of the acute disease form[45][6][20][5][4]. As animals age the likelihood of developing the acute disease form lessens therefore mortality decreases; however, producers may note a reduction in feed conversion and weight gain post-disease recovery[20][5].

Diagnosis of exudative epidermitis is often made based on the characteristic brown lesions that progress to crusting ulcers along with the other clinical signs mentioned above[20].

Prevention of Disease

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Vaccine

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A vaccine can be used for prevention of infection with S. hyicus.[46] The vaccine is made using the genes that encode exfoliative toxin type B (ExhB) from S. hyicus strains.[46] Since there is no commercial vaccine available yet, the vaccine used is an autogenous vaccine.[46][11] The vaccine uses the strain of S. hyicus that is currently affecting the herd of pigs to ensure immunity is developed to the strain within the barn. [11] The vaccine reduces the chance that pigs will die from the disease and can help reduce the use of antimicrobials to treat exudative epidermitis.[46] Vaccinated sows can pass on antibodies to the piglets so that the piglets have some passive immunity to S. hyicus. [11]

Management of pigs

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S. hyicus can enter the skin of pigs through any cut. Managing the pigs so they are unable to bite each other or ensuring the flooring is soft can decrease infection.[12] The barn should be disinfected and cleaned regularily to ensure bacteria cannot grow as easily.[11] Any new sows entering the barn should be washed to reduce contamination.[11] Teeth clipping may be necessary to reduce bite wounds in piglets.[12] When the first signs of disease is noticed, changing the bedding can reduce contamination as well as moving the pigs to a new stall.[12] Using sterile needles for injections and controlling mange may also decrease infection.[12] Exudative epidermitis is contagious between pigs and quick isolation can reduce the chance of the disease spreading.[12] Ensuring biosecurity of the farm and isolating any new pigs before introducing them to the herd can reduce transmission.[12] For young piglets, reducing the chance of chilling can impact how sick the piglets will get. [11] Keeping the barn dry and clean as well as ensuring there is adequate ventilation and humidity can decrease the amount of S. hyicus that can grow in the barn and possibly infect pigs.[11]

Treatment

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Treatments for exudative epidermitis include antibiotics given topically or injected, disinfectants, and topical oils which can relieve symptoms.[15][11] In farms which are "antibiotic-free", pigs which fall ill are removed from the production system rather than treated.[15] Farmers generally treat infected pigs topically with sprays or oils.[15] Sprays can have antibiotics such as Novobiocin and procaine penicillin G.[15] Any pigs which are dehydrated may need fluids and electrolytes to become rehydrated.[11] Rehydration is crucial as dehydration is the common cause of death in infected pigs.[11]

Staphylococcus hyicus was found to be susceptible to many antibiotics including; Norfloxacin[12][13], Ciprofloxacin[12][13], Streptomycin[12], ampicillin[13], Cephalexin[13], oxytetracycline[13] and, Gentamycin[12][13]. These antibiotics could be used to treat pigs infected with Staphylococcus hyicus. [12][13] Novobiocin and Enrofloxacin have been shown to be effective in controlling S. hyicus in vitro [14] S. hyicus is often susceptible to Vancomycin as this antibiotic is still effective against most methicillin-resistant Staphylococci.[47] With antibiotic resistance increasing in all bacteria, sending samples to a diagnostic lab for susceptibility testing is important for choosing the right antibiotic in that case. [14][48][11][47] Ensuring bacteria do not develop resistance to many antimicrobials is important for both animal and human health. [48] This is especially true in food animals, such as pigs, because resistant bacteria responsible for many common foodborne illnesses in people may be linked to animal antimicrobial resistance. [48]

References

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  1. ^ a b c d e f g h i j k l m n o p q r Frana, Timothy, Hau, Samantha (2019). Diseases of Swine, Eleventh Edition. Edited by Jeffrey J. Zimmerman, Locke A. Karriker, Alejandro Ramirez, Kent J. Schwartz, Gregory W. Stevenson, and Jianqiang Zhang. (Eleventh edition ed.). Hoboken, NJ: John Wiley & Sons, Inc. pp. 926–930. ISBN 978-1-119-35090-3. OCLC 1051779035. {{cite book}}: |edition= has extra text (help); line feed character in |others= at position 88 (help)CS1 maint: multiple names: authors list (link)
  2. ^ Devriese, LA; Derycke, J (May 1979). "Staphylococcus hyicus in cattle". Research in Veterinary Science. 26 (3): 356–8. doi:10.1016/S0034-5288(18)32893-5. PMID 515523.
  3. ^ Devriese, L. A.; Vlaminck, K.; Nuytten J. Keersmaecker Ph. (1 July 1983). "Staphylococcus hyicus in skin lesions of horses". Equine Veterinary Journal. 15 (3): 263–265. doi:10.1111/j.2042-3306.1983.tb01786.x.
  4. ^ a b c d e Andresen, Lars Ole (1 April 1998). "Differentiation and distribution of three types of exfoliative toxin produced by pigs with exudative epidermitis". FEMS Immunology & Medical Microbiology. 20 (4): 301–310. doi:10.1111/j.1574-695X.1998.tb01140.x.
  5. ^ a b c d e f g h i j k l m Merck Veterinary Manual: Overview of Exudative Epidermitis (Greasy pig disease) - https://www.merckvetmanual.com/integumentary-system/exudative-epidermitis/overview-of-exudative-epidermitis
  6. ^ a b c d e Nishifuji, K., Sugai, M., Amagai, M. (January 2008). "Staphylococcal exfoliative toxins: "Molecular scissors" of bacteria that attack the cutaneous defense barrier in mammals". Journal of Dermatological Science. 49(1): 21–31 – via ScienceDirect.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  7. ^ a b c Casanova, Carlo; Iselin, Lukas; Steiger, Niklaus von; Droz, Sara; Sendi, Parham (2011-12-01). "Staphylococcus hyicus Bacteremia in a Farmer". Journal of Clinical Microbiology. 49 (12): 4377–4378. doi:10.1128/JCM.05645-11. ISSN 0095-1137. PMC 3233007. PMID 21998429.{{cite journal}}: CS1 maint: PMC format (link)
  8. ^ a b Foissac, Maud; Lekaditi, Maria; Loutfi, Bouchra; Ehrhart, Agnès; Dauchy, Frédéric-Antoine (2016-09-01). "Spondylodiscitis and bacteremia due to Staphylococcus hyicus in an immunocompetent man". Germs. 6 (3): 106–110. doi:10.11599/germs.2016.1097. ISSN 2248-2997. PMC 5018387. PMID 27622163.
  9. ^ a b Laber, Kathy E.; Whary, Mark T.; Bingel, Sarah A.; Goodrich, James A.; Smith, Alison C.; Swindle, M. Michael (2002-01-01), Fox, James G.; Anderson, Lynn C.; Loew, Franklin M.; Quimby, Fred W. (eds.), "Chapter 15 - Biology and Diseases of Swine", Laboratory Animal Medicine (Second Edition), American College of Laboratory Animal Medicine, Burlington: Academic Press, pp. 615–673, doi:10.1016/b978-012263951-7/50018-1, ISBN 978-0-12-263951-7, PMC 7158357, retrieved 2020-10-05{{citation}}: CS1 maint: PMC format (link)
  10. ^ a b Aarestrup, Frank Møller; Jensen, Lars Bogø (2002). "Trends in antimicrobial susceptibility in relation to antimicrobial usage and presence of resistance genes in Staphylococcus hyicus isolated from exudative epidermitis in pigs". Veterinary Microbiology. 89 (1): 83–94. doi:10.1016/S0378-1135(02)00177-3.
  11. ^ a b c d e f g h i j k l Diseases of swine. Zimmerman, Jeffrey J. (10th ed ed.). Chichester, West Sussex: Wiley-Blackwell. 2012. ISBN 978-0-8138-2267-9. OCLC 757838376. {{cite book}}: |edition= has extra text (help)CS1 maint: others (link)
  12. ^ a b c d e f g h i j k l Victor I., Akwuobu C. A., Akinleye O. A., Tyagher J. A., Buba E. (2013). "Management of exudative epidermitis in 4 week old piglets" (PDF). Journal of Veterinary Medicine and Animal Health. 5 (7): 180–185 – via Academic Journals.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  13. ^ a b c d e f g h i Rajkhowa, S., Pegu, S. R., Mrinalee Devi, Kaushik, P., Anubrata Das (2011). "Occurrence of exudative epidermitis in pigs and its treatment". Indian Journal of Animal Sciences. 81 (7): 700–701 – via Web of Science.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  14. ^ a b c Wegener, H.C.; Watts, J.L.; Salmon, S.A.; Yancey, R.J. (1994). "Antimicrobial Susceptibility of Staphylococcus hyicus Isolated from Exudative Epidermitis in Pigs" (PDF). Journal of Clinical Microbiology. 32(3): 793–795.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  15. ^ a b c d e Park, J.; Friendship, R.M.; Poljak, Z. Weese, J.S.; Dewey, C.E. (2013). "An investigation of exudative epidermitis (greasy pig disease) and antimicrobial resistance patterns of Staphylococcus hyicus and Staphylococcus aureus isolated from clinical cases". The Canadian Veterinary Journal. 54(2): 139–144.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  16. ^ a b VARALDO, P. E.; HAJEK, V.; CANEPARI, P.; SATTA, G. (1985-09-01). "Additional Differentiating Characters of the Two Subspecies of Staphylococcus hyicus". Microbiology. 131 (9): 2231–2235. doi:10.1099/00221287-131-9-2231. ISSN 1350-0872.
  17. ^ Devriese, L. A.; Hajek, V.; Oeding, P.; Meyer, S. A.; Schliefer, K. H. (1 October 1978). "Staphylococcus hyicus (Sompolinsky 1953) comb. nov. and Staphylococcus hyicus subsp. chromogenes subsp. nov". International Journal of Systematic Bacteriology. 28 (4): 482–490. doi:10.1099/00207713-28-4-482.
  18. ^ Hájek, V.; Devriese, L. A.; Mordarski, M.; Goodfellow, M.; Pulverer, G.; Varaldo, P. E. (1986-10-01). "Elevation of Staphylococcus hyicus subsp. chromogenes (Devriese et al., 1978) to species status: Staphylococcus chromogenes (Devriese et al., 1978) comb. nov". Systematic and Applied Microbiology. 8 (3): 169–173. doi:10.1016/S0723-2020(86)80071-6. ISSN 0723-2020.
  19. ^ a b c d e "Staphylococcus hyicus subsp. (hyicus)". VetBact. Swedish University of Agricultural Sciences - Faculty of Veterinary Medicine and Animal Science. 2015-12-09. Retrieved 2020-10-06.{{cite web}}: CS1 maint: url-status (link)
  20. ^ a b c d e f g h i j k l m n o p q r s t Neumann, E.J., Ramirez, A., Schwartz, K.J. "Diseases Caused by Bacteria, Mycoplasmas and Spirochetes". Swine Disease Manual, Fifth Edition. American Association of Swine Veterinarians. pp. 27–28.{{cite book}}: CS1 maint: multiple names: authors list (link)
  21. ^ a b c d e f g h i j Lämmler, C (1991). "Characterization of Staphylococcus hyicus with the ATB 32 Staph system and with conventional tests". Journal of Clinical Microbiology. 29 (6): 1221–1224. doi:10.1128/jcm.29.6.1221-1224.1991. ISSN 0095-1137.
  22. ^ a b c Hassler, Ch.; Nitzsche, S.; Iversen, C.; Zweifel, C.; Stephan, R. (2008-10). "Characteristics of Staphylococcus hyicus strains isolated from pig carcasses in two different slaughterhouses". Meat Science. 80 (2): 505–510. doi:10.1016/j.meatsci.2008.02.001. {{cite journal}}: Check date values in: |date= (help)
  23. ^ a b Adkins, P. R. F.; Middleton, J. R.; Calcutt, M. J.; Stewart, G. C.; Fox, L. K. (2017-06-01). "Species Identification and Strain Typing of Staphylococcus agnetis and Staphylococcus hyicus Isolates from Bovine Milk by Use of a Novel Multiplex PCR Assay and Pulsed-Field Gel Electrophoresis". Journal of Clinical Microbiology. 55 (6): 1778–1788. doi:10.1128/JCM.02239-16. ISSN 0095-1137. PMID 28330895.
  24. ^ Takahashi, Tatsufumi; Satoh, Itona; Kikuchi, Naoya (1999-04-01). "NOTE". International Journal of Systematic and Evolutionary Microbiology. 49 (2): 725–728. doi:10.1099/00207713-49-2-725. ISSN 1466-5026.
  25. ^ "Staphylococcus hyicus gene for 16S rRNA, partial sequence, strain: ATCC 11249". 2008-08-27. {{cite journal}}: Cite journal requires |journal= (help)
  26. ^ Sasaki, Takashi; Tsubakishita, Sae; Tanaka, Yoshikazu; Sakusabe, Arihito; Ohtsuka, Masayuki; Hirotaki, Shintaro; Kawakami, Tetsuji; Fukata, Tsuneo; Hiramatsu, Keiichi (2010-03). "Multiplex-PCR Method for Species Identification of Coagulase-Positive Staphylococci". Journal of Clinical Microbiology. 48 (3): 765–769. doi:10.1128/JCM.01232-09. ISSN 0095-1137. PMC 2832457. PMID 20053855. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link)
  27. ^ Calcutt, Michael J.; Foecking, Mark F.; Hsieh, Hsin-Yeh; Adkins, Pamela R. F.; Stewart, George C.; Middleton, John R. (2015-02-26). "Sequence Analysis of Staphylococcus hyicus ATCC 11249 T , an Etiological Agent of Exudative Epidermitis in Swine, Reveals a Type VII Secretion System Locus and a Novel 116-Kilobase Genomic Island Harboring Toxin-Encoding Genes". Genome Announcements. 3 (1): e01525–14, /ga/3/1/e01525–14.atom. doi:10.1128/genomeA.01525-14. ISSN 2169-8287. PMC 4335327. PMID 25700402.{{cite journal}}: CS1 maint: PMC format (link)
  28. ^ Ladhani, Shamez; Joannou, Christopher L.; Lochrie, Denise P.; Evans, Robert W.; Poston, Susan M. (1999-04-01). "Clinical, Microbial, and Biochemical Aspects of the Exfoliative Toxins Causing Staphylococcal Scalded-Skin Syndrome". Clinical Microbiology Reviews. 12 (2): 224–242. doi:10.1128/cmr.12.2.224. ISSN 1098-6618.
  29. ^ Sato, H.; Watanabe, T.; Murata, Y.; Ohtake, A.; Nakamura, M.; Aizawa, C.; Saito, H.; Maehara, N. (1999). "New exfoliative toxin produced by a plasmid-carrying strain of Staphylococcus hyicus". Infection and Immunity. 67 (8): 4014–4018. doi:10.1128/IAI.67.8.4014-4018.1999. ISSN 0019-9567. PMC 96690. PMID 10417168.{{cite journal}}: CS1 maint: PMC format (link)
  30. ^ Sato, Hisaaki; Watanabe, Takao; Higuchi, Kohichi; Teruya, Kuniaki; Ohtake, Ayumi; Murata, Yasuko; Saito, Hiroshi; Aizawa, Chikara; Danbara, Hirofumi; Maehara, Nobutoshi (2000-07-15). "Chromosomal and Extrachromosomal Synthesis of Exfoliative Toxin from Staphylococcus hyicus". Journal of Bacteriology. 182 (14): 4096–4100. doi:10.1128/JB.182.14.4096-4100.2000. ISSN 1098-5530. PMC 94597. PMID 10869090.{{cite journal}}: CS1 maint: PMC format (link)
  31. ^ a b c Ahrens, Peter; Andresen, Lars Ole (2004-03-15). "Cloning and Sequence Analysis of Genes Encoding Staphylococcus hyicus Exfoliative Toxin Types A, B, C, and D". Journal of Bacteriology. 186 (6): 1833–1837. doi:10.1128/JB.186.6.1833-1837.2004. ISSN 0021-9193. PMC 355961. PMID 14996814.{{cite journal}}: CS1 maint: PMC format (link)
  32. ^ Amtsberg, G. (2010). "Nachweis von Exfoliation auslösenden Substanzen in Kulturen von Staphylococcus hyicus des Schweines und Staphylococcus epidermidis Biotyp 2 des Rindes". Zentralblatt für Veterinärmedizin Reihe B. 26 (4): 257–272. doi:10.1111/j.1439-0450.1979.tb00814.x. ISSN 0931-2021.
  33. ^ a b c d e Werckenthin, Christiane; Cardoso, Marisa; Martel, Jean-Louis; Schwarz, Stefan (2001). "Antimicrobial resistance in staphylococci from animals with particular reference to bovine Staphylococcus aureus, porcine Staphylococcus hyicus, and canine Staphylococcus intermedius". Veterinary Research. 32 (3–4): 341–362. doi:10.1051/vetres:2001129. ISSN 0928-4249.
  34. ^ a b Park, Jeonghwa; Friendship, Robert M; Weese, J; Poljak, Zvonimir; Dewey, Cate E (2013). "An investigation of resistance to β-lactam antimicrobials among staphylococci isolated from pigs with exudative epidermitis". BMC Veterinary Research. 9 (1): 211. doi:10.1186/1746-6148-9-211. ISSN 1746-6148.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  35. ^ Ramirez, Alejandro (2018-01-01). "Diseases affecting pigs: an overview of common bacterial, viral and parasitic pathogens of pigs". Achieving sustainable production of pig meat: Animal health and welfare. 3: 3–29. doi:10.19103/AS.2017.0013.14.
  36. ^ Torrison, Jerry; Cameron, Ranald (2019), "Integumentary System", Diseases of Swine, John Wiley & Sons, Ltd, pp. 292–312, doi:10.1002/9781119350927.ch17, ISBN 978-1-119-35092-7, retrieved 2020-10-05
  37. ^ Adkins, P. R. F.; Middleton, J. R.; Calcutt, M. J.; Stewart, G. C.; Fox, L. K. (2017-06-01). "Species Identification and Strain Typing of Staphylococcus agnetis and Staphylococcus hyicus Isolates from Bovine Milk by Use of a Novel Multiplex PCR Assay and Pulsed-Field Gel Electrophoresis". Journal of Clinical Microbiology. 55 (6): 1778–1788. doi:10.1128/JCM.02239-16. ISSN 0095-1137. PMID 28330895.
  38. ^ "Intramammary infections with different non-aureus staphylococci in dairy cows". Journal of Dairy Science. 101 (2): 1403–1418. 2018-02-01. doi:10.3168/jds.2017-13467. ISSN 0022-0302.
  39. ^ Szafraniec, Gustaw M.; Szeleszczuk, Piotr; Dolka, Beata (8-26-2020). "A Review of Current Knowledge on Staphylococcus agnetis in Poultry". Animals. 10 (8): 1421. doi:10.3390/ani10081421. {{cite journal}}: Check date values in: |date= (help)CS1 maint: unflagged free DOI (link)
  40. ^ Devriese, L. A.; Uyttebroek, E.; Dom, P.; de Herdt, P.; Ducatelle, R.; Haesebrouck, F. (1992-09). "Staphylococcus hyicus associated with pox in chickens and in turkeys". Avian Pathology. 21 (3): 529–533. doi:10.1080/03079459208418873. ISSN 0307-9457. {{cite journal}}: Check date values in: |date= (help)
  41. ^ Martins, Paula Dalcin; de Almeida, Taiana Trindade; Basso, Ana Paula; de Moura, Tiane Martin; Frazzon, Jeverson; Tondo, Eduardo César; Frazzon, Ana Paula Guedes (2013-09). "Coagulase-positive staphylococci isolated from chicken meat: pathogenic potential and vancomycin resistance". Foodborne Pathogens and Disease. 10 (9): 771–776. doi:10.1089/fpd.2013.1492. ISSN 1556-7125. PMID 23841655. {{cite journal}}: Check date values in: |date= (help)
  42. ^ Osman, Kamelia; Badr, Jihan; Al-Maary, Khalid S.; Moussa, Ihab M. I.; Hessain, Ashgan M.; Girah, Zeinab M. S. Amin; Abo-shama, Usama H.; Orabi, Ahmed; Saad, Aalaa (2016). "Prevalence of the Antibiotic Resistance Genes in Coagulase-Positive-and Negative-Staphylococcus in Chicken Meat Retailed to Consumers". Frontiers in Microbiology. 7. doi:10.3389/fmicb.2016.01846. ISSN 1664-302X.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  43. ^ Devriese, L. A.; Vlaminck, Kathleen; Nuytten, J.; Keersmaecker, Ph De (1983). "Staphylococcus hyicus in skin lesions of horses". Equine Veterinary Journal. 15 (3): 263–265. doi:10.1111/j.2042-3306.1983.tb01786.x. ISSN 2042-3306.
  44. ^ Devriese, L. A.; Nzuambe, Daya; Godard, C. (1985-04-01). "Identification and characteristics of staphylococci isolated from lesions and normal skin of horses". Veterinary Microbiology. 10 (3): 269–277. doi:10.1016/0378-1135(85)90052-5. ISSN 0378-1135.
  45. ^ a b Ladhami, S. (June 2001). "Recent developments in staphylococcal scalded skin syndrome". Clinical Microbiology and Infection. 7(6): 301 – via ProQuest.
  46. ^ a b c d Arsenakis I., Boyen F., Haesebrouck F., and Maes D.G. (2018). "Autogenous vaccination reduces antimicrobial usage and mortality rates in a herd facing severe exudative epidermitis outbreaks in weaned pigs" (PDF). Veterinary Record. 182 (26): 744–745.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  47. ^ a b Veterinary microbiology. McVey, D. Scott., Kennedy, Melissa (Melissa Anne), 1959-, Chengappa, M. M. (3rd ed. ed.). Ames, Iowa: Wiley-Blackwell. 2013. ISBN 978-0-470-95949-7. OCLC 826123137. {{cite book}}: |edition= has extra text (help)CS1 maint: others (link)
  48. ^ a b c Canada, Health (2002-09-06). "Uses of Antimicrobials in Food Animals in Canada: Impact on Resistance and Human Health [Health Canada, 2002]". aem. Retrieved 2020-10-25.

Further reading

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  • Khan, Mohammad Mubashir Ahmad d; Ashshi, Ahmad Mohammad; Faiz, Aftab (January 2014). "Clinically significant coagulase negative staphylococci and their antibiotic resistance pattern in a tertiary care hospital". Journal of Pakistan Medical Association. 304 (1): 51–62. doi:10.1016/j.ijmm.2013.09.003.
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