NOROVIRUS INFECTION (SYSTEMATIC REVIEW)

The share of norovirus infection is 17–20% of all cases of acute gastroenteritis in the world. The dominant II genogroup of noroviruses is characterized by rapid variability. The new recombinant norovirus GII.P16-GII.2 caused a sharp increase in the incidence of gastroenteritis in Asian and European countries during the winter season 2016–2017. The epidemiological features of norovirus infection are long-term excretion of the pathogen from the body of patients and carriers of viruses, especially in persons with immunosuppression; the implementation of various transmission routes (food, water, contact, aerosol), high contagiosity, winter seasonality in the countries of the northern hemisphere. In recent years, two human systems for the cultivation of noroviruses in vitro have been created, a double tropism of noroviruses has been established for immune cells and epithelial cells of the intestine, and the life cycle of noroviruses has been studied. The microbiota and its members can be either protective or stimulating for norovirus infection. Lactobacillus may play a protective role against norovirus infection. The existence of chronic norovirus infection lasting from several months to several years is proved, especially in patients with immunodeficiency. Severe form of norovirus infection and deaths are more often recorded in young children, the elderly, patients with comorbidity and immunocompromised individuals. The clinical picture of norovirus gastroenteritis is similar in many respects to other viral gastroenteritis, which determines the need for laboratory verification of the diagnosis. The polymerase chain reaction method with reverse transcription is the most widely used in the world for diagnosing infection in patients and for detecting the virus in food and environmental objects. There are still no approved vaccines and antiviral drugs against this infection. Recommended therapeutic interventions include, along with rehydration with hypoosmolar solutions, the administration of specific probiotics such as Lactobacillus GG or Saccharomyces boulardii, diosmectit and racecadotril.

1. Desselberger U. Rotaviruses. Virus Res. 2014; 190: 75-96.

2. Ahmed SM, Hall AJ, Robinson AE, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014; 14(8):725-730.

3. Blanco A, Guix S, Fuster N, et al. Norovirus in Bottled Water Associated with Gastroenteritis Outbreak, Spain, 2016. Emerg Infect Dis. 2017; 23(9):1531-1534.

4. Zhang Z, Lai S, Yu J, et al. Etiology of acute diarrhea in the elderly in China: A six-year observational study. PLoS One. 2017; 12(3):e0173881.

5. Bruun T, Salamanca BV, Bekkevold T, et al. Norwegian Enhanced Pediatric Immunisation Surveillance (NorEPIS) Network. Burden of Rotavirus Disease in Norway: Using National Registries for Public Health Research. Pediatr Infect Dis J. 2016; 35(4):396-400.

6. Gosudarstvennyj doklad “O sostojanii sanitarno-jepidemiologicheskogo blagopoluchija naselenija v Rossijskoj Federacii 2016”, 2017, pp.103-105

7. Oude Munnink BB, van der Hoek L. Viruses Causing Gastroenteritis: The Known, The New and Those Beyond. Viruses. 2016; 8(2): pii E42.

8. Nguyen GT, Phan K, Teng I, Pu J, Watanabe T. A systematic review and meta-analysis of the prevalence of norovirus in cases of gastroenteritis in developing countries. Medicine (Baltimore). 2017;96(40):e8139.

9. Ahmed SM, Lopman BA and Levy KA Systematic Review and Meta-Analysis of the Global Seasonality of Norovirus. PLoS One. 2013; 8(10): e75922.

10. Hall AJ, Lopman BA, Payne DC, et al. Norovirus disease in the United States. Emerg Infect Dis. 2013; 19:1198–1205.

11. Woodward J., Gkrania-Klotsas E., Kumararatne D. Chronic norovirus infection and common variable immunodeficiency. Clin Exp Immunol. 2017; 188(3):363–370.

12. Brown LK, Clark I, Brown JR, et al. Norovirus infection in primary immune deficiency. Rev Med Virol. 2017.[Epub ahead of print] Review. PubMed PMID: 28271593.

13. Adler JL, Zickl R. 1969. Winter vomiting disease. J Infect Dis 1969;119: 668–673.

14. Kapikian AZ, Wyatt RG, Dolin R, et al. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. 1972. J Virol 10:1075–1081.

15. Vega E, Barclay L, Gregoricus N, et al. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J Clin Microbiol. 2014;52(1):147-155.

16. Siebenga JJ, Vennema H, Renckens B, et al. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol. 2007;81(18):9932-9941.

17. Debbink K, Costantini V, Swanstrom J, et al. Human norovirus detection and production, quantification, and storage of virus-like particles. Curr Protoc Microbiol. 2013; 5; PubMed PMID:24510290; PubMed Central PMCID: PMC3920292

18. Eden JS, Hewitt J, Lim KL, et al. The emergence and evolution of the novel epidemic norovirus GII.4 variant Sydney 2012. Virology. 2014; 450-451:106-113.

19. Kwok K, Niendorf S, Lee N, et al. Increased Detection of Emergent Recombinant Norovirus GII.P16-GII.2 Strains in Young Adults, Hong Kong, China, 2016-2017. Emerg Infect Dis. 2017; 23(11):1852-1855.

20. Klinicheskie rekomendacii (protokol lechenija) okazanija medicinskoj pomoshhi detjam bol’nym norovirusnoj infekciej FGBU NIIDI FMBA ROSSII, Obshhestvennaja organizacija «Evroaziatskoe obshhestvo po infekcionnym boleznjam», Obshhestvennaja organizacija «Associacija vrachej infekcionistov Sankt-Peterburga i Leningradskoj oblasti» (AVISPO) – 2015 – 86.

21. Glass I, Parashar UD, Estes MK, Norovirus Gastroenteritis. N Engl J Med. 2009; 361(18): 1776-1785.

22. Hassard F, Sharp JH, Taft H, et al. Critical Review on the Public Health Impact of Norovirus Contamination in Shellfish and the Environment: A UK Perspective. Food Environ Virol.2017; 9(2):123-141.

23. Teunis PF, Rutjes SA, Westrell T, de Roda Husman AM. Characterization of drinking water treatment for virus risk assessment. Water Res. 2009; 43(2):395-404.

24. Atmar RL, Opekun AR, Gilger MA, et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis. 2008; 14:1553–1557.

25. Michel A., FitzGerald R., Whyte D., et al. Norovirus outbreak associated with a hotel in the west of Ireland. Eurosurveillance 2007; 12(7): е11-2.

26. Kauppinen A, Miettinen IT. Persistence of Norovirus GII Genome in Drinking Water and Wastewater at Different Temperatures. Pathogens. 2017; 6(4): pii e48.

27. Lee HM, Lee JH, Kim SH, et al. Correlation between changes in microbial/physicochemical properties and persistence of human norovirus during cabbage Kimchi fermentation. J Microbiol Biotechnol. 2017 Oct 11. doi:10.4014/ jmb.1707.07041

28. Heijne JC, Teunis P, Morroy G, et al. Enhanced hygiene measures and norovirus transmission during an outbreak. Emerg Infect Dis. 2009; 15(1):24-30.

29. Lopman B, Vennema H, Kohli E, et al. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet. 2004; 363(9410):682-688.

30. Chadwick PR, Beards G, Brown D, et al. Management of hospital outbreaks of gastro-enteritis due to small roundstructured viruses. J Hosp Infect. 2000;45(1):1-10.

31. Chenar SS, Deng Z. Development of genetic programming-based model for predicting oyster norovirus outbreak risks. Water Res. 2017; 128: 20-37.

32. Kraut RY, Snedeker KG, Babenko O, Honish L. Influence of School Year on Seasonality of Norovirus Outbreaks in Developed Countries. Can J Infect Dis Med Microbiol. 2017; 12; 10.1155/2017/9258140.

33. Bartnicki E, Cunha JB, Kolawole AO, Wobus CE. Recent advances in understanding noroviruses. F1000Res. 2017; 26; 6:79. doi:10.12688/f1000research.10081.1.eCollection

34. Bok K, Parra GI, Mitra T, et al.: Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci U S A. 2011;108(1):325–330.

35. Jones MK, Grau KR, Costantini V, et al. : Human norovirus culture in B cells. Nat Protoc. 2015; 10(12):1939–1947.

36. Kolawole AO, Rocha-Pereira J, Elftman MD, et al.: Inhibition of human norovirus by a viral polymerase inhibitor in the B cell culture system and in the mouse model. Antiviral Res. 2016;132:46–49.

37. Dolin R, Levy AG, Wyatt RG, et al. Viral gastroenteritis induced by the Hawaii agent. Jejunal histopathology and serologic response. Am J Med. 1975; 59(6):761–768.

38. Troeger H, Loddenkemper C, Schneider T, et al.: Structural and functional changes of the duodenum in human norovirus infection. Gut. 2009; 58(8):1070–1077.

39. Ettayebi K, Crawford SE, Murakami K, et al. : Replication of human noroviruses in stem cell-derived human enteroids. Science. 2016;353(6306):1387–1393.

40. Karandikar UC, Crawford SE, Ajami NJ, et al.: Detection of human norovirus in intestinal biopsies from immunocompromised transplant patients. J Gen Virol. 2016; 97(9):2291–300.

41. Thorne LG, Goodfellow IG. Norovirus gene expression and replication. J Gen Virol. 2014 Feb;95(Pt 2):278-291.

42. Perry JW, Taube S, Wobus CE. Murine norovirus-1 entry into permissive macrophages and dendritic cells is pH-independent. Virus Res. 2009; 143(1):125-129.

43. Denison MR. Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol. 2008;6(10): e270. doi: 10.1371/journal.pbio.0060270.

44. Jones MK, Watanabe M, Zhu S, et al. : Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014; 346(6210):755–759.

45. Li D, Breiman A, le Pendu J, et al.: Binding to histo-blood group antigen-expressing bacteria protects human norovirus from acute heat stress. Front Microbiol. 2015; 6:659.

46. Kernbauer E, Ding Y, Cadwell K: An enteric virus can replace the beneficial function of commensal bacteria. Nature. 2014; 516(7529):94–108.

47. Nagata S, Asahara T, Ohta T, et al. Effect of the continuous intake of probiotic-fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the faecal microflora in a health service facility for the aged. Br J Nutr. 2011;1 06(4):549–556.

48. Lee H, Ko G: Antiviral effect of vitamin A on norovirus infection via modulation of the gut microbiome. Sci Rep. 2016; 6: 25835. doi:10.1038/srep25835.

49. Brown JR, Roy S, Tutill H, et al. Super-infections and relapses occur in chronic norovirus infections. J Clin Virol. 2017:20; 96:44-48. .

50. Tomov VT, Palko O, Lau CW, et al. Differentiation and Protective Capacity of Virus-Specific CD8(+) T Cells Suggest Murine Norovirus Persistence in an Immune-Privileged Enteric Niche. Immunity. 2017; 47(4): 723-738.

51. He T, McMillen TA, Qiu Y, et al. Norovirus Loads in Stool Specimens of Cancer Patients with Norovirus Gastroenteritis. J Mol Diagn. 2017; 19(6): 836-842.

52. Dolin R, Reichman RC, Roessner KD, et al. Detection by immune electron microscopy of the Snow Mountain agent of acute viral gastroenteritis. J Infect Dis 1982; 146:184-189.

53. Dolin R, Treanor JJ, Madore HP. Novel agents of viral enteritis in humans. J Infect Dis 1987; 155:365-376.

54. Shestakova I.V. Norovirusnaja infekcija (Norovirus infections), Consilium Medicum; 2013, N12, pp.34-37.

55. Desai R, Hembree CD, Handel A, et al. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clin Infect Dis. 2012.55(2):189-193.

56. Robilotti E, Deresinski S, Pinsky BA. Norovirus. Clin Microbiol Rev. 2015; 28(1):134-64.

57. Krasnova E.I.et al. Kliniko-laboratornye osobennosti ostryh virusnyh gastrojenteritov u vzroslyh zhitelej Novosibirska (clinical and laboratory features of acute viral gastroenteritis in adults, residents of novosibirsk), Jeksperimental’naja i klinicheskaja gastrojenterologija, 2016, N9 (133), pp.14-18.

58. Dimitriadis A, Marshall JA. Evaluation of a commercial enzyme immunoassay for detection of norovirus in outbreak specimens. Eur J Clin Microbiol Infect Dis. 2005; 24:615-618.

59. Richards AF, Lopman B, Gunn A, et al. Evaluation of a commercial ELISA for detecting Norwalk-like virus antigen in faeces. J Clin Virol 2003; 26:109-115.

60. Zajko S.D. Immunohimicheskaja diagnostika norovirusnoj infekcii (Current diagnosis of infections gastroenteritis caused by norovirus), Kliniko-laboratornyj konsilium, 2009, N5, pp. 67-71.

61. Beuret C. Simultaneous detection of enteric viruses by multiplex real-time RT-PCR. J Virol Methods 2004; 115:1-8.

62. Beal SG, Tremblay EE, Toffel S, et al. A gastrointestinal PCR panel improves clinical management and lowers healthcare costs. J Clin Microbiol. 2017. pii: JCM.01457-17

63. Hartard C, Leclerc M, Rivet R, et al. F-specific RNA bacteriophages, especially members of subgroup II, should be reconsidered as good indicators of viral pollution of oysters. Appl Environ Microbiol. 2017 Oct 27. pii: AEM.01866-17

64. Guarino A, Ashkenazi S, Gendrel D, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition/ European Society for Pediatric Infectious Diseases evidencebased guidelines for the management of acute gastroenteritis in children in Europe: update 2014. J Pediatr Gastroenterol Nutr. 2014; 59(1):132-152.

65. Chen Z. Sosnovtsev SV, Bok K, et al. Development of Norwalk virus-specific monoclonal antibodies with therapeutic potential for the treatment of Norwalk virus gastroenteritis. J Virol 2013: 87:9547–9557.

66. Galasiti Kankanamalage AC, Weerawarna PM, Kim Y, et al. Anti-norovirus therapeutics: a patent review (2010-2015). Expert Opin Ther Pat. 2016; 26(3):297-308.