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