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Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients

Year 2024, Volume: 14 Issue: 3, 863 - 867, 30.09.2024
https://doi.org/10.33808/clinexphealthsci.1478430

Abstract

Objective: In this study we aimed to evaluate the prevalence of norovirus genogroups I and II and C.difficile coinfection among patients with gastroenteritis symptoms.
Method: A total of 76 patients with diarrhea were included in the study. Of these, 40 are children (<18y), 23 are adults between the ages of 18-65y, and 13 are patients older than 65 years. All these were C.difficile toxin GDH/Toxin A+B (BIOTEC, Spain) positive. In these toxin positive stool samples, Norovirus GI and GII antigen was studied by 2 methods; i.ELISA (R Biopharm, Darmstadt, Germany) and ii.polymerase chain reaction (RT – PCR). We compared the results of the antigen test (ELISA) with those of PCR for the detection of norovirus in stool
specimens. SPSS 19.0 statistical program was used to evaluate the data of the research.
Results: Out of 76 stool samples tested, 3 (3.9%) were positive for norovirus by ELISA. Subsequent RT-PCR identified norovirus GI and GII in 7 samples (9.2%). Concerning RT-PCR, the sensitivity of the ELISA test was 42.8%, and the specificity was found as 96%.
Conclusion: The study identified a 9.2% rate of co-infection with C. difficile and norovirus, with this co-infection being particularly prevalent in children. This finding emphasizes the critical need to consider both co-infection and C. difficile infection as potential causes of diarrhea in hospitalized patients, especially those under 18 or over 65 years old.

Ethical Statement

The study was approved by Marmara University Ethics Committee (Approval no. 14.01.2019-13).

Supporting Institution

This study was supported by a grant from Marmara University Scien- tific Research Commission, with grant number SAG-C-YLP-120619-0209.

Project Number

Grant number SAG-C-YLP-120619-0209.

References

  • Centers for Disease Control and Prevention. Preventing C. diff. Published [23 April 2024]. Accessed [01 May 2024] https://www.cdc.gov/c-diff/prevention/index.html
  • Korhonen L, Cohen J, Gregoricus N, Farley MM, Perlmutter R, Holzbauer SM, Dumyati G, Beldavs Z, Paulick A, Vinjé J, Limbago BM, Lessa FC, Guh AY. Evaluation of viral co-infections among patients with community-associated Clostridioides difficile infection. PLoS One. 2020;15(10):e0240549. DOI:10.1371/journal. pone. 0240549
  • World Health Organization. Immunization, Vaccines and Biologicals. Published [30 April 2022]. Accessed [01 May 2022]. https://www.who.int/teams/immunization-vaccines-and-biologicals/diseases/norovirus
  • Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346(2):312-323. DOI:10.1016/j. virol.2005.11.015
  • Bull RA, White PA. Mechanisms of GII.4 norovirus evolution. Trends Microbiol. 2011;19(5):233-240. DOI:10.1016/j.tim.2011.01.002
  • Marshall JA, Bruggink LD. The dynamics of norovirus outbreak epidemics: Recent insights. Int J Environ Res Public Health. 2011;8(4):1141-1149. DOI:10.3390/ijerph8041141
  • Del Prete R, Ronga L, Addati G, Magrone R, Abbasciano A, Decimo M, Miragliotta G. Clostridium difficile: A review on an emerging infection. Clin Ter. 2019;170(1):e41-e47. DOI:10.7417/CT.2019.2106
  • Stockmann C, Rogatcheva M, Harrel B, Vaughn M, Crisp R, Poritz M, Thatcher S, Korgenski EK, Barney T, Daly J, Pavia AT. How well does physician selection of microbiologic tests identify Clostridium difficile and other pathogens in paediatric diarrhoea? Insights using multiplex PCR-based detection. Clin Microbiol Infect. 2015;21(2): 179.e9-179.e1.79E15. DOI:10.1016/j.cmi.2014.07.011
  • Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: A systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725-730. DOI:10.1016/S1473-3099(14)70767-4
  • El Feghaly RE, Stauber JL, Tarr PI, Haslam DB. Viral co-infections are common and are associated with higher bacterial burden in children with clostridium difficile infection. J Pediatr Gastroenterol Nutr. 2013;57(6):813-816. DOI:10.1097/MPG.0b013e3182a3202f
  • Chang H, Zhang L, Ge Y, Cai J, Wang X, Huang Z, Guo J, Xu H, Gu Z, Chen H, Xu X, Zeng M. A Hospital-based Case-control Study of Diarrhea in Children in Shanghai. Pediatr Infect Dis J. 2017;36(11):1057-1063. DOI:10.1097/INF.0000000000001562
  • Skyum F, Pedersen C, Andersen V, Chen M, Franke A, Petersen D, Ries W, Mogensen CB. Risk factors for contagious gastroenteritis in adult patients with diarrhoea in the emergency department: A prospective observational multicentre study. BMC Infect Dis. 2019;19(1):133. DOI:10.1186/s12879-019-3754-4
  • Ridascreen® enzyme immunoassay platforms. Product overview. Norovirus. Accessed [01 May 2024]. https://clinical.r-biopharm.com/technologies/elisa/
  • Lees EA, Carrol ED, Ellaby NAF, Roberts P, Corless CE, Lenzi L, Darby A, O'Brien SJ, Cunliffe NA, Turner MA, Miyajima F, Pirmohamed M. Characterization of circulating Clostridium difficile strains, host response and intestinal microbiome in hospitalized children with diarrhea. Pediatr Infect Dis J. 2020;39(3):221-228. DOI:10.1097/INF.0000000000002559
  • Hall AJ, Wikswo ME, Manikonda K, Roberts VA, Yoder JS, Gould LH. Acute gastroenteritis surveillance through the National Outbreak Reporting System. United States. Emerg Infect Dis. 2013;19(8):1305-1309. DOI:10.3201/eid1908.130482
  • Stokely JN, Niendorf S, Taube S, Hoehne M, Young VB, Rogers MA, Wobus CE. Prevalence of human norovirus and Clostridium difficile coinfections in adult hospitalized patients. Clin Epidemiol. 2016;8:253-260. DOI:10.2147/CLEP.S106495
  • Korhonen L, Cohen J, Gregoricus N, Farley MM, Perlmutter R, Holzbauer SM, Dumyati G, Beldavs Z, Paulick A, Vinjé J, Limbago BM, Lessa FC, Guh AY Evaluation of viral co-infections among patients with community-associated Clostridioides difficile infection. PLoS One. 2020;15(10):e0240549. DOI:10.1371/journal. pone. 0240549
  • Murphy CN, Fowler RC, Iwen PC, Fey PD. Evaluation of the BioFire FilmArray® Gastrointestinal Panel in a Midwestern Academic Hospital. Eur J Clin Microbiol Infect Dis. 2017;36(4):747-754. DOI:10.1007/s10096-016-2858-7
  • de Graaf H, Pai S, Burns DA, Karas JA, Enoch DA, Faust SN. Co-infection as a confounder for the role of Clostridium difficile infection in children with diarrhoea: A summary of the literature. Eur J Clin Microbiol Infect Dis. 2015;34(7):1281-1287. DOI:10.1007/s10096-015-2367-0
  • Mattner F, Guyot A, Henke-Gendo C. Analysis of norovirus outbreaks reveals the need for timely and extended microbiological testing. J Hosp Infect. 2015;91(4):332-337. DOI:10.1016/j. jhin.2015.08.020
  • Johnson S, Lavergne V, Skinner AM, Gonzales-Luna AJ, Garey KW, Kelly CP, Wilcox MH. Clinical Practice Guideline by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA): 2021 Focused Update Guidelines on Management of Clostridioides difficile Infection in Adults. Clin Infect Dis. 2021;73(5):e1029-e1044. DOI:10.1093/cid/ciab549
  • Yang S, Li M, Cheng J, Wan G, Zhou Y, Jia H, Wei H, Song R, Sheng L, Wang H, Wang L, Hua W. Diagnostic determination of Norovirus infection as one of the major causes of infectious diarrhea in HIV patients using a multiplex polymerase chain reaction assay. Int J STD AIDS. 2019;30(6):550-556. DOI:10.1177/0956462418824912
Year 2024, Volume: 14 Issue: 3, 863 - 867, 30.09.2024
https://doi.org/10.33808/clinexphealthsci.1478430

Abstract

Project Number

Grant number SAG-C-YLP-120619-0209.

References

  • Centers for Disease Control and Prevention. Preventing C. diff. Published [23 April 2024]. Accessed [01 May 2024] https://www.cdc.gov/c-diff/prevention/index.html
  • Korhonen L, Cohen J, Gregoricus N, Farley MM, Perlmutter R, Holzbauer SM, Dumyati G, Beldavs Z, Paulick A, Vinjé J, Limbago BM, Lessa FC, Guh AY. Evaluation of viral co-infections among patients with community-associated Clostridioides difficile infection. PLoS One. 2020;15(10):e0240549. DOI:10.1371/journal. pone. 0240549
  • World Health Organization. Immunization, Vaccines and Biologicals. Published [30 April 2022]. Accessed [01 May 2022]. https://www.who.int/teams/immunization-vaccines-and-biologicals/diseases/norovirus
  • Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346(2):312-323. DOI:10.1016/j. virol.2005.11.015
  • Bull RA, White PA. Mechanisms of GII.4 norovirus evolution. Trends Microbiol. 2011;19(5):233-240. DOI:10.1016/j.tim.2011.01.002
  • Marshall JA, Bruggink LD. The dynamics of norovirus outbreak epidemics: Recent insights. Int J Environ Res Public Health. 2011;8(4):1141-1149. DOI:10.3390/ijerph8041141
  • Del Prete R, Ronga L, Addati G, Magrone R, Abbasciano A, Decimo M, Miragliotta G. Clostridium difficile: A review on an emerging infection. Clin Ter. 2019;170(1):e41-e47. DOI:10.7417/CT.2019.2106
  • Stockmann C, Rogatcheva M, Harrel B, Vaughn M, Crisp R, Poritz M, Thatcher S, Korgenski EK, Barney T, Daly J, Pavia AT. How well does physician selection of microbiologic tests identify Clostridium difficile and other pathogens in paediatric diarrhoea? Insights using multiplex PCR-based detection. Clin Microbiol Infect. 2015;21(2): 179.e9-179.e1.79E15. DOI:10.1016/j.cmi.2014.07.011
  • Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, Koopmans M, Lopman BA. Global prevalence of norovirus in cases of gastroenteritis: A systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725-730. DOI:10.1016/S1473-3099(14)70767-4
  • El Feghaly RE, Stauber JL, Tarr PI, Haslam DB. Viral co-infections are common and are associated with higher bacterial burden in children with clostridium difficile infection. J Pediatr Gastroenterol Nutr. 2013;57(6):813-816. DOI:10.1097/MPG.0b013e3182a3202f
  • Chang H, Zhang L, Ge Y, Cai J, Wang X, Huang Z, Guo J, Xu H, Gu Z, Chen H, Xu X, Zeng M. A Hospital-based Case-control Study of Diarrhea in Children in Shanghai. Pediatr Infect Dis J. 2017;36(11):1057-1063. DOI:10.1097/INF.0000000000001562
  • Skyum F, Pedersen C, Andersen V, Chen M, Franke A, Petersen D, Ries W, Mogensen CB. Risk factors for contagious gastroenteritis in adult patients with diarrhoea in the emergency department: A prospective observational multicentre study. BMC Infect Dis. 2019;19(1):133. DOI:10.1186/s12879-019-3754-4
  • Ridascreen® enzyme immunoassay platforms. Product overview. Norovirus. Accessed [01 May 2024]. https://clinical.r-biopharm.com/technologies/elisa/
  • Lees EA, Carrol ED, Ellaby NAF, Roberts P, Corless CE, Lenzi L, Darby A, O'Brien SJ, Cunliffe NA, Turner MA, Miyajima F, Pirmohamed M. Characterization of circulating Clostridium difficile strains, host response and intestinal microbiome in hospitalized children with diarrhea. Pediatr Infect Dis J. 2020;39(3):221-228. DOI:10.1097/INF.0000000000002559
  • Hall AJ, Wikswo ME, Manikonda K, Roberts VA, Yoder JS, Gould LH. Acute gastroenteritis surveillance through the National Outbreak Reporting System. United States. Emerg Infect Dis. 2013;19(8):1305-1309. DOI:10.3201/eid1908.130482
  • Stokely JN, Niendorf S, Taube S, Hoehne M, Young VB, Rogers MA, Wobus CE. Prevalence of human norovirus and Clostridium difficile coinfections in adult hospitalized patients. Clin Epidemiol. 2016;8:253-260. DOI:10.2147/CLEP.S106495
  • Korhonen L, Cohen J, Gregoricus N, Farley MM, Perlmutter R, Holzbauer SM, Dumyati G, Beldavs Z, Paulick A, Vinjé J, Limbago BM, Lessa FC, Guh AY Evaluation of viral co-infections among patients with community-associated Clostridioides difficile infection. PLoS One. 2020;15(10):e0240549. DOI:10.1371/journal. pone. 0240549
  • Murphy CN, Fowler RC, Iwen PC, Fey PD. Evaluation of the BioFire FilmArray® Gastrointestinal Panel in a Midwestern Academic Hospital. Eur J Clin Microbiol Infect Dis. 2017;36(4):747-754. DOI:10.1007/s10096-016-2858-7
  • de Graaf H, Pai S, Burns DA, Karas JA, Enoch DA, Faust SN. Co-infection as a confounder for the role of Clostridium difficile infection in children with diarrhoea: A summary of the literature. Eur J Clin Microbiol Infect Dis. 2015;34(7):1281-1287. DOI:10.1007/s10096-015-2367-0
  • Mattner F, Guyot A, Henke-Gendo C. Analysis of norovirus outbreaks reveals the need for timely and extended microbiological testing. J Hosp Infect. 2015;91(4):332-337. DOI:10.1016/j. jhin.2015.08.020
  • Johnson S, Lavergne V, Skinner AM, Gonzales-Luna AJ, Garey KW, Kelly CP, Wilcox MH. Clinical Practice Guideline by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA): 2021 Focused Update Guidelines on Management of Clostridioides difficile Infection in Adults. Clin Infect Dis. 2021;73(5):e1029-e1044. DOI:10.1093/cid/ciab549
  • Yang S, Li M, Cheng J, Wan G, Zhou Y, Jia H, Wei H, Song R, Sheng L, Wang H, Wang L, Hua W. Diagnostic determination of Norovirus infection as one of the major causes of infectious diarrhea in HIV patients using a multiplex polymerase chain reaction assay. Int J STD AIDS. 2019;30(6):550-556. DOI:10.1177/0956462418824912
There are 22 citations in total.

Details

Primary Language English
Subjects Clinical Microbiology
Journal Section Articles
Authors

Hanife Şura Şalcı Aslan 0000-0002-1832-8325

Fatih Mehmet Akıllı 0000-0001-8541-7742

Elvan Sayin 0000-0002-1320-1704

Arzu Akşit İlki 0000-0003-3887-7003

Project Number Grant number SAG-C-YLP-120619-0209.
Early Pub Date September 27, 2024
Publication Date September 30, 2024
Submission Date May 4, 2024
Acceptance Date August 2, 2024
Published in Issue Year 2024 Volume: 14 Issue: 3

Cite

APA Şalcı Aslan, H. Ş., Akıllı, F. M., Sayin, E., Akşit İlki, A. (2024). Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients. Clinical and Experimental Health Sciences, 14(3), 863-867. https://doi.org/10.33808/clinexphealthsci.1478430
AMA Şalcı Aslan HŞ, Akıllı FM, Sayin E, Akşit İlki A. Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients. Clinical and Experimental Health Sciences. September 2024;14(3):863-867. doi:10.33808/clinexphealthsci.1478430
Chicago Şalcı Aslan, Hanife Şura, Fatih Mehmet Akıllı, Elvan Sayin, and Arzu Akşit İlki. “Prevalence of Norovirus Coinfection in Clostridioides Difficile Toxin Positive Patients”. Clinical and Experimental Health Sciences 14, no. 3 (September 2024): 863-67. https://doi.org/10.33808/clinexphealthsci.1478430.
EndNote Şalcı Aslan HŞ, Akıllı FM, Sayin E, Akşit İlki A (September 1, 2024) Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients. Clinical and Experimental Health Sciences 14 3 863–867.
IEEE H. Ş. Şalcı Aslan, F. M. Akıllı, E. Sayin, and A. Akşit İlki, “Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients”, Clinical and Experimental Health Sciences, vol. 14, no. 3, pp. 863–867, 2024, doi: 10.33808/clinexphealthsci.1478430.
ISNAD Şalcı Aslan, Hanife Şura et al. “Prevalence of Norovirus Coinfection in Clostridioides Difficile Toxin Positive Patients”. Clinical and Experimental Health Sciences 14/3 (September 2024), 863-867. https://doi.org/10.33808/clinexphealthsci.1478430.
JAMA Şalcı Aslan HŞ, Akıllı FM, Sayin E, Akşit İlki A. Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients. Clinical and Experimental Health Sciences. 2024;14:863–867.
MLA Şalcı Aslan, Hanife Şura et al. “Prevalence of Norovirus Coinfection in Clostridioides Difficile Toxin Positive Patients”. Clinical and Experimental Health Sciences, vol. 14, no. 3, 2024, pp. 863-7, doi:10.33808/clinexphealthsci.1478430.
Vancouver Şalcı Aslan HŞ, Akıllı FM, Sayin E, Akşit İlki A. Prevalence of Norovirus Coinfection in Clostridioides difficile Toxin Positive Patients. Clinical and Experimental Health Sciences. 2024;14(3):863-7.

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