Predictors of Clostridium difficile infection severity in patients hospitalised in medical intensive care

World Journal of Gastroenterology

Volumn 19, Issue 44, 2013, Pages 8034-8041

  Khanafer, Nagham ^a,b   Touré, Abdoulaye ^a,b   Chambrier, Cécile ^a   Cour, Martin ^b,c   Reverdy, Marie Elisabeth ^d   Argaud, Laurent ^c   Vanhems, Philippe ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b EDOUARD HERRIOT HOSPITAL   (France)

^c CROIX ROUSSE HOSPITAL   (France)

^d Hospices Civils de Lyon   (France)

Author keywords

Clostridium difficile; Health care associated infection; Hospital acquired infection; Intensive care unit; Nosocomial infection; Severe clostridium difficile infection

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; C REACTIVE PROTEIN; CEPHALOSPORIN; METRONIDAZOLE; PIPERACILLIN PLUS TAZOBACTAM; QUINOLONE DERIVATIVE; STOMACH SECRETION INHIBITOR; VANCOMYCIN;

ABDOMINAL PAIN; ADULT; AGED; ARTICLE; BODY MASS; CLINICAL ARTICLE; CLOSTRIDIUM DIFFICILE INFECTION; COHORT ANALYSIS; DIABETES MELLITUS; DIARRHEA; DISEASE SEVERITY; FEVER; GENDER; HOSPITAL INFECTION; HOSPITALIZATION; HUMAN; INTENSIVE CARE UNIT; LENGTH OF STAY; MALE; MORBIDITY; MORTALITY; PREDICTIVE VALUE; PROGNOSIS; RETROSPECTIVE STUDY; RISK FACTOR;

CLOSTRIDIUM DIFFICILE; HEALTH-CARE ASSOCIATED INFECTION; HOSPITAL-ACQUIRED INFECTION; INTENSIVE CARE UNIT; NOSOCOMIAL INFECTION; SEVERE CLOSTRIDIUM DIFFICILE INFECTION;

AGED; ANTI-BACTERIAL AGENTS; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; CHI-SQUARE DISTRIBUTION; CLOSTRIDIUM DIFFICILE; CROSS INFECTION; ENTEROCOLITIS, PSEUDOMEMBRANOUS; FEMALE; FRANCE; HOSPITALIZATION; HOSPITALS, UNIVERSITY; HUMANS; INCIDENCE; INTENSIVE CARE UNITS; LOGISTIC MODELS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; ODDS RATIO; PROGNOSIS; RETROSPECTIVE STUDIES; RISK FACTORS; SEVERITY OF ILLNESS INDEX; SEX FACTORS; UP-REGULATION;

EID: 84888621749     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i44.8034     Document Type: Article

References (54)

1. Kuijper EJ, Coignard B, Tüll P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006; 12 Suppl 6: 2-18 [PMID: 16965399]
2. Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S, Bourgault AM, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson TJ, Horn R, René P, Monczak Y, Dascal A. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 2005; 353: 2442-2449 [PMID: 16322602]
3. Muto CA, Pokrywka M, Shutt K, Mendelsohn AB, Nouri K, Posey K, Roberts T, Croyle K, Krystofiak S, Patel-Brown S, Pasculle AW, Paterson DL, Saul M, Harrison LH. A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 2005; 26: 273-280 [PMID: 15796280]
4. Pépin J, Valiquette L, Alary ME, Villemure P, Pelletier A, Forget K, Pépin K, Chouinard D. Clostridium difficileassociated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 2004; 171: 466-472 [PMID: 15337727]
5. Pindera L. C. difficile inquest too narrow as "Quebec strain" goes international. CMAJ 2007; 176: 915-916 [PMID: 17389432]
6. Ricciardi R, Rothenberger DA, Madoff RD, Baxter NN. Increasing prevalence and severity of Clostridium difficile colitis in hospitalized patients in the United States. Arch Surg 2007; 142: 624-31; discussion 631 [PMID: 17638799]
7. Bobo LD, Dubberke ER, Kollef M. Clostridium difficile in the ICU: the struggle continues. Chest 2011; 140: 1643-1653 [PMID: 22147824 DOI: 10.1378/chest.11-0556]
8. Sinaii N. Charting the course for the future of science in healthcare epidemiology: results of a survey of the membership of the Society of Healthcare Epidemiology of America. Infect Control Hosp Epidemiol 2010; 31: 669-675 [PMID: 20482374 DOI: 10.1086/653203]
9. Kenneally C, Rosini JM, Skrupky LP, Doherty JA, Hollands JM, Martinez E, McKinzie WE, Murphy T, Smith JR, Micek ST, Kollef MH. Analysis of 30-day mortality for clostridium difficile-associated disease in the ICU setting. Chest 2007; 132: 418-424 [PMID: 17573523]
10. McDonald LC, Killgore GE, Thompson A, Owens RC, Kazakova SV, Sambol SP, Johnson S, Gerding DN. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 2005; 353: 2433-2441 [PMID: 16322603]
11. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, Frost E, McDonald LC. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005; 366: 1079-1084 [PMID: 16182895]
12. Carignan A, Allard C, Pépin J, Cossette B, Nault V, Valiquette L. Risk of Clostridium difficile infection after perioperative antibacterial prophylaxis before and during an outbreak of infection due to a hypervirulent strain. Clin Infect Dis 2008; 46: 1838-1843 [PMID: 18462108 DOI: 10.1086/588291]
13. Dial S, Delaney JA, Schneider V, Suissa S. Proton pump inhibitor use and risk of community-acquired Clostridium difficile-associated disease defined by prescription for oral vancomycin therapy. CMAJ 2006; 175: 745-748 [PMID: 17001054]
14. Kyne L, Sougioultzis S, McFarland LV, Kelly CP. Underlying disease severity as a major risk factor for nosocomial Clostridium difficile diarrhea. Infect Control Hosp Epidemiol 2002; 23: 653-659 [PMID: 12452292]
15. Owens RC, Donskey CJ, Gaynes RP, Loo VG, Muto CA. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin Infect Dis 2008; 46 Suppl 1: S19-S31 [PMID: 18177218 DOI: 10.1086/521859]
16. Pant C, Madonia P, Minocha A. Does PPI therapy predispose to Clostridium difficile infection? Nat Rev Gastroenterol Hepatol 2009; 6: 555-557 [PMID: 19713988 DOI: 10.1038/ nrgastro.2009.128]
17. van der Kooi TI, Koningstein M, Lindemans A, Notermans DW, Kuijper E, van den Berg R, Boshuizen H, Filius PM, van den Hof S. Antibiotic use and other risk factors at hospital level for outbreaks with Clostridium difficile PCR ribotype 027. J Med Microbiol 2008; 57: 709-716 [PMID: 18480327 DOI: 10.1099/jmm.0.47711-0]
18. Dubberke ER, Butler AM, Reske KA, Agniel D, Olsen MA, D' Angelo G, McDonald LC, Fraser VJ. Attributable outcomes of endemic Clostridium difficile-associated disease in nonsurgical patients. Emerg Infect Dis 2008; 14: 1031-1038 [PMID: 18598621 DOI: 10.3201/eid1407.070867]
19. Gravel D, Miller M, Simor A, Taylor G, Gardam M, McGeer A, Hutchinson J, Moore D, Kelly S, Boyd D, Mulvey M. Health care-associated Clostridium difficile infection in adults admitted to acute care hospitals in Canada: a Canadian Nosocomial Infection Surveillance Program Study. Clin Infect Dis 2009; 48: 568-576 [PMID: 19191641 DOI: 10.1086/596703]
20. Karas JA, Enoch DA, Aliyu SH. A review of mortality due to Clostridium difficile infection. J Infect 2010; 61: 1-8 [PMID: 20361997 DOI: 10.1016/j.jinf.2010.03.025]
21. Pépin J, Valiquette L, Cossette B. Mortality attributable to nosocomial Clostridium difficile-associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 2005; 173: 1037-1042 [PMID: 16179431]
22. Redelings MD, Sorvillo F, Mascola L. Increase in Clostridium difficile-related mortality rates, United States, 1999-2004. Emerg Infect Dis 2007; 13: 1417-1419 [PMID: 18252127 DOI: 10.3201/eid1309.061116]
23. Sánchez-Somolinos M, Alcalá L, Peláez T, Marín M, Martín A, Catalán P, Bouza E. High levels of resistance to fluoroquinolones among Clostridium difficile isolates in a Spanish hospital. Clin Infect Dis 2008; 47: 818-822 [PMID: 18680418 DOI: 10.1086/591201]
24. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000-2005. Emerg Infect Dis 2008; 14: 929-931 [PMID: 18507904 DOI: 10.3201/eid1406.071447]
25. Peery AF, Dellon ES, Lund J, Crockett SD, McGowan CE, Bulsiewicz WJ, Gangarosa LM, Thiny MT, Stizenberg K, Morgan DR, Ringel Y, Kim HP, Dibonaventura MD, Carroll CF, Allen JK, Cook SF, Sandler RS, Kappelman MD, Shaheen NJ. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012; 143: e1-3 [PMID: 22885331]
26. Lawrence SJ, Puzniak LA, Shadel BN, Gillespie KN, Kollef MH, Mundy LM. Clostridium difficile in the intensive care unit: epidemiology, costs, and colonization pressure. Infect Control Hosp Epidemiol 2007; 28: 123-130 [PMID: 17265392]
27. O'Brien JA, Lahue BJ, Caro JJ, Davidson DM. The emerging infectious challenge of clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol 2007; 28: 1219-1227 [PMID: 17926270]
28. McEllistrem MC, Carman RJ, Gerding DN, Genheimer CW, Zheng L. A hospital outbreak of Clostridium difficile disease associated with isolates carrying binary toxin genes. Clin Infect Dis 2005; 40: 265-272 [PMID: 15655746]
29. Weber DJ, Raasch R, Rutala WA. Nosocomial infections in the ICU: the growing importance of antibiotic-resistant pathogens. Chest 1999; 115: 34S-41S [PMID: 10084458]
30. Musa SA, Moran C, Thomson SJ, Cowan ML, McAnulty G, Grounds M, Rahman TM. Clostridium difficile-associated disease acquired in the cardiothoracic intensive care unit. J Cardiothorac Vasc Anesth 2011; 25: 263-267 [PMID: 20638863 DOI: 10.1053/j.jvca]
31. Musa SA, Robertshaw H, Thomson SJ, Cowan ML, Rahman TM. Clostridium difficile-associated disease acquired in the neurocritical care unit. Neurocrit Care 2010; 13: 87-92 [PMID: 20443154 DOI: 10.1007/s12028-010-9374-x]
32. Comission Nationale de l'Informatique et des Libertés. Available from: URL: http://www.cnil.fr/english/the-cnil/status/
33. Institut de Veille Sanitaire. Available from: URL: http://www.invs.sante.fr/publications/2006/guide_raisin/conduite_clostridiumdifficile.pdf. 2006
34. Haute Autorité de la Santé. Available from: URL: http://www.has-sante.fr/portail/upload/docs/application/pdf/denutrition_recos_2006_09_25__14_20_46_375.pdf. 2003
35. Abrahamian FM, Talan DA, Moran GJ, Pinner R. Update on emerging infections from the Centers for Disease Control and Prevention. Severe Clostridium difficile-associated disease in populations previously at low risk--four states, 2005. Ann Emerg Med 2006; 48: 55-59 [PMID: 16791928]
36. Kuijper EJ, van Dissel JT, Wilcox MH. Clostridium difficile: changing epidemiology and new treatment options. Curr Opin Infect Dis 2007; 20: 376-383 [PMID: 17609596]
37. Sheth SG, LaMont JT. Gastrointestinal problems in the chronically critically ill patient. Clin Chest Med 2001; 22: 135-147 [PMID: 11315452]
38. Leclair MA, Allard C, Lesur O, Pépin J. Clostridium difficile infection in the intensive care unit. J Intensive Care Med 2010; 25: 23-30 [PMID: 20034951 DOI: 10.1177/885066609350871]
39. Serón-Arbeloa C, Puzo-Foncillas J, Garcés-Gimenez T, Escós-Orta J, Labarta-Monzón L, Lander-Azcona A. A retrospective study about the influence of early nutritional support on mortality and nosocomial infection in the critical care setting. Clin Nutr 2011; 30: 346-350 [PMID: 21131108 DOI: 10.1016/j.clnu.2010.11.004]
40. Heyland DK, MacDonald S, Keefe L, Drover JW. Total parenteral nutrition in the critically ill patient: a meta-analysis. JAMA 1998; 280: 2013-2019 [PMID: 9863853]
41. Linsky A, Gupta K, Lawler EV, Fonda JR, Hermos JA. Proton pump inhibitors and risk for recurrent Clostridium difficile infection. Arch Intern Med 2010; 170: 772-778 [PMID: 20458084 DOI: 10.1001/archinternmed.2010.73]
42. Howell MD, Novack V, Grgurich P, Soulliard D, Novack L, Pencina M, Talmor D. Iatrogenic gastric acid suppression and the risk of nosocomial Clostridium difficile infection. Arch Intern Med 2010; 170: 784-790 [PMID: 20458086 DOI: 10.1001/archintermed]
43. Hardt C, Berns T, Treder W, Dumoulin FL. Univariate and multivariate analysis of risk factors for severe Clostridium difficile-associated diarrhoea: importance of co-morbidity and serum C-reactive protein. World J Gastroenterol 2008; 14: 4338-4341 [PMID: 18666322]
44. Morrison RH, Hall NS, Said M, Rice T, Groff H, Brodine SK, Slymen D, Lederman ER. Risk factors associated with complications and mortality in patients with Clostridium difficile infection. Clin Infect Dis 2011; 53: 1173-1178 [PMID: 21976459 DOI: 10.1093/cid/cir668]
45. Henrich TJ, Krakower D, Bitton A, Yokoe DS. Clinical risk factors for severe Clostridium difficile-associated disease. Emerg Infect Dis 2009; 15: 415-422 [PMID: 19239754 DOI: 10.3201/eid1503.080312]
46. Lamontagne F, Labbé AC, Haeck O, Lesur O, Lalancette M, Patino C, Leblanc M, Laverdière M, Pépin J. Impact of emergency colectomy on survival of patients with fulminant Clostridium difficile colitis during an epidemic caused by a hypervirulent strain. Ann Surg 2007; 245: 267-272 [PMID: 17245181]
47. Peled N, Pitlik S, Samra Z, Kazakov A, Bloch Y, Bishara J. Predicting Clostridium difficile toxin in hospitalized patients with antibiotic-associated diarrhea. Infect Control Hosp Epidemiol 2007; 28: 377-381 [PMID: 17385141]
48. Wanahita A, Goldsmith EA, Musher DM. Conditions associated with leukocytosis in a tertiary care hospital, with particular attention to the role of infection caused by clostridium difficile. Clin Infect Dis 2002; 34: 1585-1592 [PMID: 12032893]
49. Ananthakrishnan AN, Guzman-Perez R, Gainer V, Cai T, Churchill S, Kohane I, Plenge RM, Murphy S. Predictors of severe outcomes associated with Clostridium difficile infection in patients with inflammatory bowel disease. Aliment Pharmacol Ther 2012; 35: 789-795 [PMID: 22360370 DOI: 10.1111/j.1365-2036.2012.05022.x]
50. Moshkowitz M, Ben-Baruch E, Kline Z, Shimoni Z, Niven M, Konikoff F. Risk factors for severity and relapse of pseudomembranous colitis in an elderly population. Colorectal Dis 2007; 9: 173-177 [PMID: 17223943]
51. Bhangu S, Bhangu A, Nightingale P, Michael A. Mortality and risk stratification in patients with Clostridium difficileassociated diarrhoea. Colorectal Dis 2010; 12: 241-246 [PMID: 19508548 DOI: 10.1111/j.1463-1318.2009.01832.x]
52. Bhangu A, Nepogodiev D, Gupta A, Torrance A, Singh P. Systematic review and meta-analysis of outcomes following emergency surgery for Clostridium difficile colitis. Br J Surg 2012; 99: 1501-1513 [PMID: 22972525 DOI: 10.1002/bjs.8868]
53. Andrews CN, Raboud J, Kassen BO, Enns R. Clostridium difficile-associated diarrhea: predictors of severity in patients presenting to the emergency department. Can J Gastroenterol 2003; 17: 369-373 [PMID: 12813602]
54. Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, Pepin J, Wilcox MH. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol 2010; 31: 431-455 [PMID: 20307191 DOI: 10.1086/651706]