Hepatic disease and the risk of mortality of Vibrio vulnificus necrotizing skin and soft tissue infections: A systematic review and meta-analysis


Autoři: Po-Yao Chuang aff001;  Tien-Yu Yang aff001;  Tsan-Wen Huang aff001;  Yao-Hung Tsai aff001;  Kuo-Chin Huang aff001;  Hsu-Huei Weng aff002
Působiště autorů: Department of Orthopaedic Surgery, Chiayi Chang Gung Memorial Hospital, Chiayi, Taiwan aff001;  Chang Gung University College of Medicine, Taoyuan, Taiwan aff002;  Department of Diagnostic Radiology, Chiayi Chang Gung Memorial Hospital, Chiayi, Taiwan aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223513

Souhrn

Background

Vibrio vulnificus necrotizing skin and soft tissue infections (VNSSTIs) are associated with a high mortality rate that varies remarkably with host susceptibility. Hepatic disease (HD) is considered the key risk factor for high VNSSTIs incidence and mortality; however, there is limited evidence in the literature to support this observation.

Methodology

We examined all reported cases of VNSSTIs and associated mortality rates between 1966 and mid-2018. The PubMed, Medline and Cochrane Library databases were systematically searched for observational studies on patients with VNSSTIs. Twelve studies with 1157 total patients with VNSSTIs were included in the analysis. From the pooled dataset, nearly half (46.8%) of the patients with VNSSTIs had HD. The mortality rate in HD patients with VNSSTIs was 53.9% (n = 292/542), which was considerably higher than the mortality rate of 16.1% (n = 99/615) in non-HD patients. Patients with HD contracted VNSSTIs were found to be two or more times (RR = 2.61, 95% CI = 2.14–3.19) as likely to die compared with those without HD. Besides, liver cirrhosis (LC), the end-stage HD, was confirmed to be a significant risk factor, with risk ratios of 1.84 (95% CI 1.21–2.79) and 2.00 (95% CI 1.41–2.85) when compared to non-LC and non-HD, respectively.

Conclusions

HD with or without LC can be associated with infections and complications from V. vulnificus. Clinicians should aggressively approach care and management of acutely and/or critically ill patients with VNSSTIs.

Klíčová slova:

Death rates – Medical risk factors – Metaanalysis – Skin infections – Skin tissue – Systematic reviews – Vibrio vulnificus – Soft tissue infections


Zdroje

1. Strom MS, Paranjpye RN. Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect. 2000; 2(2): 177–188. 10742690

2. Gulig PA, Bourdage KL, Starks AM. Molecular pathogenesis of Vibrio vulnificus. J Microbiol. 2005; 43: 118–131. 15765065

3. Diaz JH. Skin and soft tissue infections following marine injuries and exposures in travelers. J Travel Med. 2014; 21(3): 207–213. doi: 10.1111/jtm.12115 24628985

4. Tsai YH, Hsu RW, Huang KC, Chen CH, Cheng CC, Peng KT, et al. Systemic Vibrio infection presenting as necrotizing fasciitis and sepsis. A series of thirteen cases. J Bone Joint Surg Am. 2004; 86(11): 2497–2502. doi: 10.2106/00004623-200411000-00021 15523024

5. Stevens DL, Bisno AL, Chambers HF, Dellinger EP, Goldstein EJ, Gorbach SL, et al. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis. 2014; 59(2): e10–52. doi: 10.1093/cid/ciu444 24973422

6. Huang KC, Hsieh PH, Huang KC, Tsai YH. Vibrio necrotizing soft-tissue infection of the upper extremity: factors predictive of amputation and death. J Infect. 2008; 57(4): 290–297. doi: 10.1016/j.jinf.2008.07.009 18755513

7. Mitra AK. Vibrio vulnificus infection: epidemiology, clinical presentations, and prevention. South Med J. 2004; 97(2): 118–119. doi: 10.1097/01.SMJ.0000092520.47509.C2 14982256

8. Haq SM, Dayal HH. Chronic liver disease and consumption of raw oysters: a potentially lethal combination—a review of Vibrio vulnificus septicemia. Am J Gastroenterol. 2005; 100(5): 1195–1199. doi: 10.1111/j.1572-0241.2005.40814.x 15842598

9. Bross MH, Soch K, Morales R, Mitchell RB. Vibrio vulnificus infection: diagnosis and treatment. Am Fam Physician. 2007; 76(4): 539–544. 17853628

10. Dechet AM, Yu PA, Koram N, Painter J. Nonfoodborne Vibrio infections: an important cause of morbidity and mortality in the United States, 1997–2006. Clin Infect Dis. 2008; 46(7): 970–976. doi: 10.1086/529148 18444811

11. Shapiro RL, Altekruse S, Hutwagner L, Bishop R, Hammond R, Wilson S, et al. The role of gulf coast oysters harvested in warmer months in Vibrio vulnificus infections in the United States, 1988–1996. J Infect Dis. 1998; 178(3): 752–759. doi: 10.1086/515367 9728544

12. Chuang YC, Yuan CY, Liu CY, Lan CK, Huang AH. Vibrio vulnificus infection in Taiwan: report of 28 cases and review of clinical manifestations and treatment. Clin Infect Dis. 1992; 15(2): 271–276. doi: 10.1093/clinids/15.2.271 1520762

13. Centers for Disease Control and Prevention (CDC). Vibrio vulnificus infections associated with raw oyster consumption: Florida, 1981–1992. Morb Mortal Wkly Rep. 1993; 42(21): 405–407.

14. Chang JJ, Sheen IS, Peng SM, Chen PC, Wu CS, Leu HS. Vibrio vulnificus infection: report of 8 cases and review of cases in Taiwan. Changgeng Yi Xue Za Zhi. 1994; 17(4): 339–346. 7850649

15. Liu JW, Lee IK, Tang HJ, Ko WC, Lee HC, Liu YC, et al. Prognostic factors and antibiotics in Vibrio vulnificus septicemia. Arch Intern Med. 2006; 166(19): 2117–2123. doi: 10.1001/archinte.166.19.2117 17060542

16. Inoue Y, Ono T, Matsui T, Miyasaka J, Kinoshita Y, Ihn H. Epidemiological survey of Vibrio vulnificus infection in Japan between 1999 and 2003. J Dermatol. 2008; 35(3): 129–139. doi: 10.1111/j.1346-8138.2008.00432.x 18346255

17. Tsai YH, Huang TJ, Hsu RW, Weng YJ, Hsu WH, Huang KC, et al. Necrotizing soft-tissue infections and primary sepsis caused by Vibrio vulnificus and Vibrio cholerae non-O1. J Trauma. 2009; 66 (3): 899–905. doi: 10.1097/TA.0b013e31816a9ed3 19276771

18. Matsumoto K, Ohshinge K, Fujita N, Tomita Y, Mitsumizo S, Nakashima M, et al. Clinical features of Vibrio vulnificus infections in the coastal areas of the Ariake Sea, Japan. J Infect Chemother. 2010; 16(4): 272–279. doi: 10.1007/s10156-010-0050-z 20229050

19. Yeung YK, Ho ST, Yen CH, Ho PC, Tse WL, Lau YK, et al. Factors affecting mortality in Hong Kong patients with upper limb necrotizing fasciitis. Hong Kong Med J. 2011; 17(2): 96–104. 21471588

20. Chao WN, Tsai CF, Chang HR, Chan KS, Su CH, Lee YT, et al. Impact of timing of surgery on outcome of Vibrio vulnificus-related necrotizing fasciitis. Am J Surg. 2013; 206(1): 32–39. doi: 10.1016/j.amjsurg.2012.08.008 23414632

21. Lee YC, Hor LI, Chiu HY, Lee JW, Shieh SJ. Prognostic factor of mortality and its clinical implications in patients with necrotizing fasciitis caused by Vibrio vulnificus. Eur J Clin Microbiol Infect Dis. 2014; 33(6): 1011–1018. doi: 10.1007/s10096-013-2039-x 24419406

22. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283(15): 2008–2012. doi: 10.1001/jama.283.15.2008 10789670

23. Genaidy AM, Lemasters GK, Lockey J, Succop P, Deddens J, Sobeih T, et al. An epidemiological appraisal instrument: a tool for evaluation of epidemiological studies. Ergonomics. 2007; 50(6): 920–960. doi: 10.1080/00140130701237667 17457750

24. Heidelbaugh JJ, Briderly M. Cirrhosis and chronic liver failure: part I. Diagnosis and evaluation. Am Fam Physician. 2006; 74(5): 756–762. 16970019

25. Seki E, Schwabe RF. Hepatic inflammation and fibrosis: functional links and key pathways. Hepatology. 2015; 61(3): 1066–1079. doi: 10.1002/hep.27332 25066777

26. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest. 2005; 115(2): 209–218. doi: 10.1172/JCI24282 15690074

27. Sohrabpour AA, Mohamadnejad M, Malekzadeh R. Review article: the reversibility of cirrhosis. Aliment Pharmacol Ther. 2012; 36(9): 824–832. doi: 10.1111/apt.12044 22966946

28. Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: in search of a pathophysiological classification of cirrhosis. Hepatology. 2010; 51(4): 1445–1449. doi: 10.1002/hep.23478 20077563

29. Heidelbaugh JJ, Sherbondy M. Cirrhosis and chronic liver failure: part II. Complications and treatment. Am Fam Physician. 2006; 74(5): 767–776. 16970020

30. Moreau R. Acute-on-chronic liver failure: a new syndrome in cirrhosis. Clin Mol Hepatol. 2016; 22(1): 1–6. doi: 10.3350/cmh.2016.22.1.1 27044760

31. Bernal W, Jalan R, Quaglia A, Simpson K, Wendon J, Burroughs A. Acute-on-chronic liver failure. Lancet. 2015; 386(10003): 1576–1587. doi: 10.1016/S0140-6736(15)00309-8 26423181

32. Ercolani G, Cucchetti A, Cescon M, Ravaioli M, Grazi GL, Pinna AD. Predictive indices of morbidity and mortality after liver resection. Ann Surg. 2006; 244(4): 635–637.

33. Huang KC, Tsai YH, Huang KC, Lee MS. Model for end-stage liver disease (MELD) as a predictor and monitor of mortality in patients with Vibrio vulnificus necrotizing skin and soft tissue infections. PLoS Negl Trop Dis. 2015; 9(4): 0003720.

34. Nakatani Y, Fukui H, Kitano H, Nagamoto I, Tsujimoto T, Kuriyama S, et al. Endotoxin clearance and its relation to hepatic and renal disturbances in rats with liver cirrhosis. Liver. 2001; 21(1): 64–70. doi: 10.1034/j.1600-0676.2001.210110.x 11169075

35. Nesseler N, Launey Y, Aninat C, Morel F, Malledant Y, Seguin P. Clinical review: The liver in sepsis. Crit Care. 2012; 16(5): 235. doi: 10.1186/cc11381 23134597

36. Powell JL, Strauss KA, Wiley C, Zhan M, Morris JG Jr. Inflammatory Cytokine Response to Vibrio vulnificus Elicited by Peripheral Blood Mononuclear Cells from Chronic Alcohol Users Is Associated with Biomarkers of Cellular Oxidative Stress. Infect Immun. 2003; 71: 4212–4216 doi: 10.1128/IAI.71.7.4212-4216.2003 12819121

37. Espat NJ, Auffenberg T, Abouhamze A, Baumhofer J, Moldawer LL, Howard R J. A role for tumor necrosis factor-alpha in the increased mortality associated with Vibrio vulnificus infection in the presence of hepatic dysfunction. Ann Surg. 1996; 223(4), 428. doi: 10.1097/00000658-199604000-00012 8633922

38. Hor LI, Chang TT, Wang ST. Survival of Vibrio vulnificus in whole blood from patients with chronic liver diseases: association with phagocytosis by neutrophils and serum ferritin levels. J Infect Dis. 1999; 179:275–8. doi: 10.1086/314554 9841854

39. Litwin CM, Calderwood SB. Cloning and genetic analysis of the Vibrio vulnificus fur gene and construction of a fur mutant by in vivo marker exchange. J Bacteriol. 1993; 175(3), 706–715. doi: 10.1128/jb.175.3.706-715.1993 7678593

40. Chae MR, Park BH, Kim JS, Rho HW, Park JW, Kim HR. Protective effect of C-reactive protein against the lethality induced by Vibrio vulnificus lipopolysaccharide. Microbiol Immunol. 2000; 44(5), 335–340. doi: 10.1111/j.1348-0421.2000.tb02503.x 10888350

41. Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol. 2006; 45(4), 529–538 doi: 10.1016/j.jhep.2006.05.013 16879891

42. Heng SP, Letchumanan V, Deng CY, Ab Mutalib NS, Khan TM, Chuah LH, et al. Vibrio vulnificus: an environmental and clinical burden. Front Microbiol. 2017; 8, 997. doi: 10.3389/fmicb.2017.00997 28620366

43. Zanetti S, Spanu T, Deriu A, Romano L, Sechi LA, Fadda G. in vitro susceptibility of Vibrio spp. Isolated from the environment. Int J Antimicrob Agents. 2001; 17(5): 407–409. doi: 10.1016/s0924-8579(01)00307-7 11337229

44. Shaw KS, Rosenberg Goldstein RE, He X, Jacobs JM, Crump BC, Sapkota AR. Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland Coastal Bays. PLoS One. 2014; 9(2): e89616. doi: 10.1371/journal.pone.0089616 24586914

45. Vaseeharan B, Ramasamy P, Murugan T, Chen JC. In vitro susceptibility of antibiotics against Vibrio spp. and Aeromonas spp. Isolated from Penaeus monodon hatcheries nd ponds. Int J Antimicrob Agents. 2005; 26(4): 285–291. doi: 10.1016/j.ijantimicag.2005.07.005 16139992

46. Huang KC, Weng HH, Yang TY, Chang TS, Huang TW, Lee MS. Distribution of fatal Vibrio vulnificus necrotizing skin and soft tissue infections: a systematic review and meta-analysis. Medicine. 2016; 95(5), e2627. doi: 10.1097/MD.0000000000002627 26844475


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