1887
Surveillance Open Access
Like 0

Abstract

Introduction

Universal vaccination of toddlers has led to very low hepatitis A (HAV) endemicity in Israel. However, sporadic outbreaks still occur, necessitating better surveillance.

Aim

To implement a comprehensive HAV surveillance programme.

Methods

In 2017 and 2018, sera from suspected HAV cases that tested positive for anti-HAV IgM antibodies were transferred to the Central Virology Laboratory (CVL) for molecular confirmation and genotyping. Sewage samples were collected in Israel and Palestine* and were molecularly analysed. All molecular (CVL), epidemiological (District Health Offices and Epidemiological Division) and clinical (treating physicians) data were combined and concordantly assessed.

Results

Overall, 146 cases (78 in 2017 and 68 in 2018, median age 34 years, 102 male) and 240 sewage samples were studied. Most cases (96%) were unvaccinated. In 2017, 89% of cases were male, 45% of whom were men who have sex with men (MSM). In 2018, 49% were male, but only 3% of them were MSM (p < 0.01). In 2017, 82% of cases and 63% of sewage samples were genotype 1A, phylogenetically associated with a global MSM-HAV outbreak. In 2018, 80% of cases and 71% of sewage samples were genotype 1B, related to the endemic strain previously identified in Israel and Palestine*. Environmental analysis revealed clustering of sewage and cases’ sequences, and country-wide circulation of HAV.

Conclusions

Molecular confirmation of HAV infection in cases and analysis of environmental samples, combined with clinical and epidemiological investigation, may improve HAV surveillance. Sequence-based typing of both clinical and sewage-derived samples could assist in understanding viral circulation.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2021.26.6.2000001
2021-02-11
2021-03-01
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2021.26.6.2000001
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/26/6/eurosurv-26-6-3.html?itemId=/content/10.2807/1560-7917.ES.2021.26.6.2000001&mimeType=html&fmt=ahah

References

  1. Lavanchy D. Viral hepatitis: global goals for vaccination. J Clin Virol. 2012;55(4):296-302.  https://doi.org/10.1016/j.jcv.2012.08.022  PMID: 22999800 
  2. American Academy of Pediatrics Committee on Infectious Diseases. Hepatitis A vaccine recommendations. Pediatrics. 2007;120(1):189-99.  https://doi.org/10.1542/peds.2007-1088  PMID: 17606579 
  3. Lemon SM, Ott JJ, Van Damme P, Shouval D. Type A viral hepatitis: A summary and update on the molecular virology, epidemiology, pathogenesis and prevention. J Hepatol. 2017;S0168-8278(17)32278-X. PMID: 28887164 
  4. Jacobsen KH. Globalization and the Changing Epidemiology of Hepatitis A Virus. Cold Spring Harb Perspect Med. 2018;8(10):a031716.  https://doi.org/10.1101/cshperspect.a031716  PMID: 29500305 
  5. Beauté J, Westrell T, Schmid D, Müller L, Epstein J, Kontio M, et al. Travel-associated hepatitis A in Europe, 2009 to 2015. Euro Surveill. 2018;23(22):1700583.  https://doi.org/10.2807/1560-7917.ES.2018.23.22.1700583  PMID: 29871720 
  6. Ndumbi P, Freidl GS, Williams CJ, Mårdh O, Varela C, Avellón A, et al. Hepatitis A outbreak disproportionately affecting men who have sex with men (MSM) in the European Union and European Economic Area, June 2016 to May 2017. Euro Surveill. 2018;23(33):1700641.  https://doi.org/10.2807/1560-7917.ES.2018.23.33.1700641  PMID: 30131095 
  7. Sachdeva H, Benusic M, Ota S, Stuart R, Maclachlan J, Dubey V, et al. Community outbreak of hepatitis A disproportionately affecting men who have sex with men in Toronto, Canada, January 2017-November 2018. Can Commun Dis Rep. 2019;45(10):262-8.  https://doi.org/10.14745/ccdr.v45i10a03  PMID: 31647057 
  8. Chen WC, Chiang PH, Liao YH, Huang LC, Hsieh YJ, Chiu CM, et al. Outbreak of hepatitis A virus infection in Taiwan, June 2015 to September 2017. Euro Surveill. 2019;24(14):1800133.  https://doi.org/10.2807/1560-7917.ES.2019.24.14.1800133  PMID: 30968822 
  9. Rivas V, Barrera A, Pino K, Núñez R, Caceres CJ, Lopez-Lastra M, et al. Hepatitis A outbreak since November 2016 affecting men who have sex with men (MSM) in Chile connected to the current outbreak in MSM in Europe, situation up to October 2017. Euro Surveill. 2018;23(9):1800060.  https://doi.org/10.2807/1560-7917.ES.2018.23.9.18-00060  PMID: 29510780 
  10. Foster MA, Hofmeister MG, Kupronis BA, Lin Y, Xia GL, Yin S, et al. Increase in Hepatitis A Virus Infections - United States, 2013-2018. MMWR Morb Mortal Wkly Rep. 2019;68(18):413-5.  https://doi.org/10.15585/mmwr.mm6818a2  PMID: 31071072 
  11. Manor Y, Lewis M, Ram D, Daudi N, Mor O, Savion M, et al. Evidence for Hepatitis A virus endemic circulation in Israel despite universal toddlers’ vaccination since 1999 and low clinical incidence in all age groups. J Infect Dis. 2016;jiw611.  PMID: 28013247 
  12. Gozlan Y, Bar-Or I, Rakovsky A, Savion M, Amitai Z, Sheffer R, et al. Ongoing hepatitis A among men who have sex with men (MSM) linked to outbreaks in Europe in Tel Aviv area, Israel, December 2016 - June 2017. Euro Surveill. 2017;22(29):30575.  https://doi.org/10.2807/1560-7917.ES.2017.22.29.30575  PMID: 28749336 
  13. Nainan OV, Xia G, Vaughan G, Margolis HS. Diagnosis of hepatitis a virus infection: a molecular approach. Clin Microbiol Rev. 2006;19(1):63-79.  https://doi.org/10.1128/CMR.19.1.63-79.2006  PMID: 16418523 
  14. National Intitute for Public Health and Environment (RIVM). Molecular detection and typing of VP1 region of HAV. Protocol. Bilthoven: RIVM; 2018. Available from: https://www.rivm.nl/sites/default/files/2018-11/Typing%20protocol%20HAVNET%20VP1P2A%20a1a.pdf
  15. Enkirch T, Severi E, Vennema H, Thornton L, Dean J, Borg ML, et al. Improving preparedness to respond to cross-border hepatitis A outbreaks in the European Union/European Economic Area: towards comparable sequencing of hepatitis A virus. Euro Surveill. 2019;24(28).  https://doi.org/10.2807/1560-7917.ES.2019.24.28.1800397  PMID: 31311618 
  16. Patel JC, Diop OM, Gardner T, Chavan S, Jorba J, Wassilak SGF, et al. Surveillance to Track Progress Toward Polio Eradication - Worldwide, 2017-2018. MMWR Morb Mortal Wkly Rep. 2019;68(13):312-8.  https://doi.org/10.15585/mmwr.mm6813a4  PMID: 30946737 
  17. Manor Y, Handsher R, Halmut T, Neuman M, Bobrov A, Rudich H, et al. Detection of poliovirus circulation by environmental surveillance in the absence of clinical cases in Israel and the Palestinian authority. J Clin Microbiol. 1999;37(6):1670-5.  https://doi.org/10.1128/JCM.37.6.1670-1675.1999  PMID: 10325305 
  18. La Rosa G, Libera SD, Iaconelli M, Ciccaglione AR, Bruni R, Taffon S, et al. Surveillance of hepatitis A virus in urban sewages and comparison with cases notified in the course of an outbreak, Italy 2013. BMC Infect Dis. 2014;14(1):419.  https://doi.org/10.1186/1471-2334-14-419  PMID: 25074676 
  19. National Institute for Public Health and the Environment (RIVM). Hepatitis A Virus Genotyping Tutorial. Bilthoven: RIVM. [Accessed: 27 Feb 2019]. Available from: https://www.rivm.nl/mpf/typingtool/hav/how-to-use
  20. Carmona G, Vilaró M, Ciruela P, Jané M, Giralt L, Ruiz L, et al. Hepatitis A surveillance: sensitivity of two information sources. BMC Infect Dis. 2018;18(1):633.  https://doi.org/10.1186/s12879-018-3552-4  PMID: 30526527 
  21. Association of Public Health Laboratories (APHL). Hepatitis A Virus Testing and Resources. Silver Spring, MD: APHL; 2018. Available from: https://www.aphl.org/programs/infectious_disease/Documents/2018_HAV_DiagnosticUpdate.pdf
  22. Bisseux M, Colombet J, Mirand A, Roque-Afonso AM, Abravanel F, Izopet J, et al. Monitoring human enteric viruses in wastewater and relevance to infections encountered in the clinical setting: a one-year experiment in central France, 2014 to 2015. Euro Surveill. 2018;23(7).  https://doi.org/10.2807/1560-7917.ES.2018.23.7.17-00237  PMID: 29471623 
  23. Hellmér M, Paxéus N, Magnius L, Enache L, Arnholm B, Johansson A, et al. Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Appl Environ Microbiol. 2014;80(21):6771-81.  https://doi.org/10.1128/AEM.01981-14  PMID: 25172863 
  24. Manor Y, Shulman LM, Kaliner E, Hindiyeh M, Ram D, Sofer D, et al. Intensified environmental surveillance supporting the response to wild poliovirus type 1 silent circulation in Israel, 2013. Euro Surveill. 2014;19(7):20708.  https://doi.org/10.2807/1560-7917.ES2014.19.7.20708  PMID: 24576473 
  25. Brouwer AF, Eisenberg JNS, Pomeroy CD, Shulman LM, Hindiyeh M, Manor Y, et al. Epidemiology of the silent polio outbreak in Rahat, Israel, based on modeling of environmental surveillance data. Proc Natl Acad Sci USA. 2018;115(45):E10625-33.  https://doi.org/10.1073/pnas.1808798115  PMID: 30337479 
  26. Konduru K, Kaplan GG. Stable growth of wild-type hepatitis A virus in cell culture. J Virol. 2006;80(3):1352-60.  https://doi.org/10.1128/JVI.80.3.1352-1360.2006  PMID: 16415012 
  27. Pellegrinelli L, Galli C, Binda S, Primache V, Tagliacarne C, Pizza F, et al. Molecular Characterization and Phylogenetic Analysis of Enteroviruses and Hepatitis A Viruses in Sewage Samples, Northern Italy, 2016. Food Environ Virol. 2019;11(4):393-9.  https://doi.org/10.1007/s12560-019-09401-4  PMID: 31420848 
/content/10.2807/1560-7917.ES.2021.26.6.2000001
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error