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

Iwata, Kentaro; Doi, Asako; Fukuchi, Takahiko; Ohji, Goh; Shirota, Yuko; Sakai, Tetsuya; Kagawa, Hiroki

doi:10.1186/1471-2334-14-247

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	Some^c	No	No	Some^d	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 TA^a	Yes	Yes^b	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	Yes^d	No	Yes (SEC and TSST-1)	No	No	Probably TSS^f
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	Probably^g	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	Yes^h	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 al^j[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	No^k
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 al^l[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

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
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.
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.
c. Among the patients identified, the analysis was done for the use of antibiotics in 30 cases.
d. The article did refer to C. difficile but did not specify the methods to identify it.
e. Seventeen out of 34 patients did have concurrent C. difficile infection.
f. The patient developed septic shock with multiple organ failure, with identification of MRSA from multiple sites.
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.
h. Randomly selected S. aureus isolates were used for comparison of toxin productions.
i. LukE-LukD are one of staphylococcal leukotoxin family [66].
j. It is possible that some patients in this paper might been described in reference 37 in duplicates.
k. The patient died of shock and organ failure. The blood culture after the death grew MRSA.
l. All isolates of S. aureus in this study was oxacillin susceptible.

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