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Table 1 Summary of Case Records and Case Series on Antibiotic Associated Enterocolitis considered to be caused by MRSA

From: A systematic review for pursuing the presence of antibiotic associated enterocolitis caused by methicillin resistant Staphylococcus aureus

Reference Year Country No. of patients Prior exposure to antibiotics Endoscopic findings c/w AAE Gram staining or other microscopic findings Presence of MRSA while excluding CDI Comparison group Toxin assay Animal model Response to the treatment Judged to be different from TSS or food poisoning
Hori et al. [8]. 1989 Japan 154 Somec No No Somed No Yes (SEC, and TSST-1) No Yes Some TSSs
McDonald et al. [23]. 1982 Australia 10 Yes Yes in 1 pt Yes Yes by CCFA cx and TA No No No Yes Yes
Christie et al. [24]. 1988 USA 1 No No No Yes by TAa Yes Yesb No Yes Yes
Sakamoto et al. [25]. 1990 Japan 1 Yes Yes No Yes by TA No Negative TSST-1 No Yes Yes
Matsuo et al. [26].e 1991 Japan 34 Yes in 28 4 patients with autopsy findings No Yes by CCFA cx. No No No Yes No
Nakashio et al. [27]. 1991 Japan 1 No No No Yesd No Yes (SEC and TSST-1) No No Probably TSSf
Takeshima et al. [28]. 1991 Japan 16 Yes No No Yes by CCMA cx. No No No No Yes
Ueda et al. [29]. 1991 Japan 2 Yes No No Yes by GDH and cx of unknown methods. No Yes (SEA and TSST-1) No Yes UC
Hanatani et al. [30]. 1992 Japan 1 Yes No Yes Yes by TA No Yes (TSST-1 coding gene) No Yes Yes
Inamatsu et al. [31]. 1992 Japan 32 Yes No No Yes by TA and cx of unknown methods. No Yes (SE and TSST-1) No Yes One pt might have had TSS
Masuda et al. [32]. 1993 Japan 1 Yes No Yes Yes by GDH No No No Yes Yes
Taylor et al. [33]. 1993 UK 1 Yes No No Yes by TA and cx of unknown methods. No Yes (SEA) No Yes Yes
Takatera et al. [34]. 1994 Japan 2 Yes No No Yes by GDH No No No Yes Yes
Kuramoto et al. [35]. 1996 Japan 16 Yes No No Yes by TA Yes No No Yes Yes
Watanabe et al. [36]. 1996 Japan 9 Yes No No Yes by GDH and cx of unknown methods. Yes No No Yes Yes
Konishi et al. [37]. 1997 Japan 31 Probablyg No No Yes by cx of unknown methods. No No No Yes Yes
Sakai et al. [38]. 1997 Japan 19 Yes No No Yes by GDH and cx of unknown methods. Compared with CDI No No No Yes
Yoshida et al. [39]. 1997 Japan 1 Yes Autopsy findings c/w multiple ulcers with abscess. No pseudomembrane formation. Yes Yes by unknown methods. No Yes (SEC) No No Yes
Schiller et al. [40]. 1998 USA 1 Yes No Yes Yes by TA No No No Yes with ineffectiveness of metronidazole. Yes
Kimata et al. [22]. 1999 Japan 1 No No No Yes by GDH No Yes (SEC, TSST-1, and protease B) No Yes Yes
Gravet et al. [41]. 1999 France 104 Yes No No Yes by CCFA and TA Yesh Yes (SEA, SED, LukE-LukDi) No Yes Yes
Terada et al. [42]. 2000 Japan 1 No No No Yes by TA No Yes (TSST-1) No Yes Yes
Watanabe et alj[43]. 2001 Japan 13 Yes No No Yes by GDH and cx of unknown methods. No Yes (SEA, SEC and TSST-1) No No Yes
Yanagi et al. [44]. 2002 Japan 1 Yes No No Yes by GDH No Yes (SEC and TSST-1) No Yes No
Igami et al. [45]. 2002 Japan 13 Yes No No Yes by GDH No No No Yes Yes
Lee et al. [46]. 2003 S. Korea 1 Yes Yes Yes Yes by TA No No No Yes Yes
Fujita et al. [47]. 2004 Japan 1 Yes Autopsy findings c/w PC with cocci Yes Yes by GDH No No No No Nok
Yoshida et al. [48]. 2004 Japan 1 Yes Yes No Yes by TA No No No No Probably necrotizing enterocolitis with Fournier gangrene.
Froberg et al. [49]. 2004 USA 1 Yes Autopsy findings c/w PC Yes. Also, PCR of pseudomembrane was positive for MRSA. Positive TA No No No No Yes
Rhee et al. [50]. 2004 USA 1 Yes No No Yes by TA No No No Yes (and no response to metronidazole) Yes
Nishizawa et al. [51]. 2005 Japan 1 Yes No No Yes by GDH No No No Yes No
Ackermann et all[52]. 2005 Germany 25 Yes No No Yes by CCFA cx and TA. Compared with CDI. Yes (SEA, SEB, SEC, and SED) No UC No
McPherson et al. [53]. 2005 UK 1 Yes No No Yes by TA No No No Yes Yes
Boyce et al. [54]. 2005 USA 11 Yes    Yes by CCFA cx Yes Yes (SEA, SEB, and SED) No Yes Yes
Asha et al. [55]. 2006 UK 10 Yes No No Yes by CCEY cx and TA. Compared with CDI and C. perfringens infections. Yes (SEA, SEC, SED and TSST-1) No UK Yes
Kurabayashi et al. [56]. 2007 Japan 1 Yes No Yes Yes by GDH No No No Yes Yes
Nagao et al. [57]. 2007 Japan 2 Yes No No positive TA (A only) in cone case. Negative in the other. No No No Yes, and no response to metronidazole. Yes
Flemming et al. [58]. 2007 Germany 29 Yes No No Yes by CCFA cx and TA With CDI. Yes (SEA, SEB, SEC, SED, and SEE) No UC Yes
Kotler et al. [59]. 2007 USA 1 No Yes Yes (Gram stain of ileal tissue and transmission electron micrograph) Yes by TA No Yes (SEB, SEC) No Yes Co-existence of TSS and enterocolitis.
Shiraishi et al. [60]. 2008 Japan 18 UC No No Yes by TA With CDI No No Yes Yes
Tamura et al. [61]. 2008 Japan 10 Yes No No Yes by GDH With CDI No No Yes Yes
Dalal et al. [62]. 2008 USA 2 Yes No Yes Yes by TA No No No Yes Yes
Lo et al. [63]. 2009 USA 5 Yes No No Yes by TA No No No Yes Yes
Fujii et al. [64]. 2010 Japan 1 UC No No Yes by TA No No No Yes Yes
Kitahata Y et al. [65]. 2011 Japan 1 Yes Yes No Yes by GDH No No No Yes Yes
  1. Abbreviations: MRSA methicillin-resistant Staphylococcus aureus, c/w consistent with, AAE antibiotic associated enterocolitis, CDI Clostridium difficile infection, TSS toxic shock syndrome, pt patient, CCFA cycloserine-cefoxitin-fructose agar, cx culture, TA toxin assay, SEC staphylococcal enterotoxin C, TSST-1 toxic shock syndrome toxin-1, CCMA cycloserine-cefoxitin-mannitol ager, GDH glutamate dehydrogenase assay, SEA staphylococcal enterotoxin A, SE staphylococcal enterotoxins, SED staphylococcal enterotoxin D, SEB staphylococcal enterotoxin B, UC unclear, PC pseudomembranous colitis, CCEY cycloserine-cefoxitin egg yolk agar, SEE staphylococcal enterotoxin E
  2. a. There was no specification whether S. aureus in this article was indeed MRSA. However, the patient was treated with oral vancomycin, suggesting it was.
  3. b. Cytopathic effects (CPE) were seen both via intracellular growth of S. aureus and with cell-free supernatant, suggesting the presence of toxin in S. aureus from the case. CPEs were not seen both in control S. aureus and its supernatant.
  4. c. Among the patients identified, the analysis was done for the use of antibiotics in 30 cases.
  5. d. The article did refer to C. difficile but did not specify the methods to identify it.
  6. e. Seventeen out of 34 patients did have concurrent C. difficile infection.
  7. f. The patient developed septic shock with multiple organ failure, with identification of MRSA from multiple sites.
  8. g. All cases are postoperative. Although there was no specific reference on the use of antibiotics, most patients in Japan usually receive varieties of antibiotics routinely after surgery, particularly in 1980s and 90s.
  9. h. Randomly selected S. aureus isolates were used for comparison of toxin productions.
  10. i. LukE-LukD are one of staphylococcal leukotoxin family [66].
  11. j. It is possible that some patients in this paper might been described in reference 37 in duplicates.
  12. k. The patient died of shock and organ failure. The blood culture after the death grew MRSA.
  13. l. All isolates of S. aureus in this study was oxacillin susceptible.