LETTERS term to dramatically reduce the high 3. Biswas PK, Christensen JP, Ahmed SS, biologically relevant sentinels and incidence of HPAI in Bangladesh. We Barua H, Das A, Rahman MH. at al. Avian can indicate potential pathogens that infl uenza outbreaks in chickens, Bangla- have progressively and dramatically desh. Emerg Infect Dis. 2008;14:1909–12. are contaminating the environment. increased the scope and benefi ts of our http://dx.doi.org/10.3201/eid1412.071567 It is essential to ensure that this pilot PVC implementation program, 4. Biswas PK, Christensen JP, Ahmed SS, sustainable resource of coastal areas, but additional work is needed. To Das A, Rahman MH, Barua H, et al. where mussels and oysters are farmed Risk for infection with highly pathogenic help spread PVC approaches through- avian infl uenza virus (H5N1) in back- or collected wild, is not subjected to out the country, community leaders, yard chickens, Bangladesh. Emerg In- environmental contamination that imams of local mosques, and school fect Dis. 2009;15:1931–6. http://dx.doi. could lead to public health risks. teachers can be trained to implement org/10.3201/eid1512.090643 Risk management for bivalve 5. Biswas PK, Rahman MH, Das A, Ahmed awareness programs on safe practices SS, Giasuddin M, Christensen JP. Risk mollusks, aimed at control of fecal for raising poultry and regular clean- for highly pathogenic avian infl uenza pollution, relies heavily on the use ing and disinfection of live bird mar- H5N1 virus infection in chickens in of Escherichia coli as an indicator kets. The strengthening of biosecurity small-scale commercial farms, in a high- of fecal (sewage) contamination risk area, Bangladesh, 2008. Transbound measures will help control the spread Emerg Dis. 2011;58:519–25. http://dx.doi. and is enacted under European food of HPAI virus and other zoonotic org/10.1111/j.1865-1682.2011.01235.x regulations (Regulation 854/2004, diseases. www.cefas.co.uk/media/455777/ Address for correspondence: Shankar P. Mondal, extract_reg_no_854_2004.pdf). Acknowledgments Department of Veterinary and Biomedical However, although these regulations We acknowledge Zakaria Noyon and Sciences, College of Veterinary Medicine, probably reduce the number of Suman Das-Gupta for providing technical University of Minnesota, St. Paul, MN 55108, infections, especially bacterial assistance in implementation of the proj- USA; email: [email protected] infections, they are not viewed as ect. We thank Paritosh K. Biswas for as- adequately controlling the risk for sisting with data analysis and for review- viral infections. Specifi c risks are ing the manuscript. posed by the robustness of viruses in the environment and the different This project was funded by the Unit- behavior of viruses within bivalve ed States Agency for International Devel- mollusks compared with behavior opment. within bacterial fecal indicators. Hepatitis E HEV is deemed to be inactivated Shankar P. Mondal, Virus Genotype 3 during processing procedures used David Tardif-Douglin, in Shellfi sh, to prepare mussels for consumption; Robert Ryan-Silva, however, HEV is only 50% inactivated and Rich Magnani United Kingdom at 56°C and 96% at 60°C for 1 Author affi liations: Development Alterna- To the Editor: Bivalve mollusks hour, it is stable when exposed to tives Inc., Bethesda, Maryland, USA (S.P. (shellfi sh), such as mussels and trifl uorotrichloroethane, and it is Mondal, D. Tardif-Douglin, R. Ryan-Silva, oysters, are fi lter feeders; they resistant to inactivation by acidic and R. Magnani); and University of Minnesota, concentrate microorganisms of human alkaline conditions (4). Most shellfi sh St. Paul, Minnesota, USA (S.P. Mondal) and animal origin (up to 100×) from are usually eaten raw, but viable virus DOI: http://dx.doi.org/10.3201/eid1812.120635 the surrounding environment. Several can also pose a risk to public health recent reports have linked the incidence in shellfi sh that are lightly steamed References of human infection with hepatitis or preserved by smoking and/or in E virus (HEV) to consumption of acetic acid. Indeed, a recent study by 1. World Health Organization for Animal the Food Standards Agency, in which Health. Update on highly pathogenic undercooked pork, game products, avian infl uenza in animals (type H5 and and shellfi sh (1,2). Infectious HEV >800 oyster samples from 39 growing H7) [cited 2012 Mar 19]. http://www.oie. has been found in swine manure and beds in the United Kingdom were int/animal-health-in-the-world/update-on- wastewater (3); therefore, application collected and screened during 2009– avian-infl uenza/2012/ 2011, found norovirus at low levels 2. World Health Organization. Cumulative of manure to land and subsequent number of confi rmed human cases of avi- runoff could contaminate coastal in at least 76% of oysters (5). Other an infl uenza A(H5N1) reported to WHO water, leading to contamination of studies identifi ed hepatitis A virus [cited 2012 Mar 19]. http://www.who. shellfi sh and, subsequently, possible and norovirus in shellfi sh production int/influenza/human_animal_interface/ areas and in ready-to-eat products in H5N1_cumulative_table_archives/en/ human infection. Because they are index.html fi lter feeders, bivalve mollusks are the United Kingdom (1,6). In fact,

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 12, December 2012 2085 LETTERS depuration experiments demonstrated the contaminated foodstuff have been and the east coast of Scotland (9 no decrease in titers against hepatitis conducted. Thus, possible transmission at Stannergate, Dundee; Ferryden, A virus over a 23-hour cleansing routes for HEV remain poorly studied Montrose; and the Ythan Estuary at period (7). In addition, acute HEV in the United Kingdom (2). Newburgh). infection attributed to consumption To determine whether HEV is The site at Ardrossan was near a of shellfi sh was diagnosed for 33 present in mussels collected locally slaughterhouse and a meat preparation passengers who recently returned from for human consumption, we examined purifi cation plant that processes pigs. a cruise (2). However, data have been 48 mussels from 5 tidal locations in The plant was considered a potential restricted to questionnaires implicating Scotland. We collected closed mussels source of contamination, and mussels consumption of shellfi sh as a source of from the west coast of Scotland (11 at were collected in a 10-m2 area around transmission; no follow-up analyses of Lunderston Bay and 28 at Ardrossan) an outfall (drain/sewage pipe) directly in line with the processing plant. A total of 36 (92%) of the 39 mussels from the west coast were positive by PCR for HEV, and 5 (55%) of the 9 from the east coast were positive. The mean value of HEV RNA detected in the samples was

4.25 log10 IU/mL (range 3.73–5.2 log10 IU/mL), and the assay was validated by using the current candidate HEV World Health Organization standard (http://whqlibdoc.who.int/hq/2011/ WHO_BS_2011.2175_eng.pdf). Phylogenetic analysis showed that most bivalve mollusk sequences clustered with HEV genotype 3 from humans and swine (Figure; online Technical Appendix, wwwnc.cdc. gov/EID/pdfs/12-0924-Techapp. pdf). Also, HEV sequences isolated specifi cally from a UK human source corresponded with sequences isolated from the bivalve mollusks. The presence of a swine-like HEV genotype 3 in freshwater bivalve mollusks has also been reported in Japan and South Korea (1,9). Worldwide, an estimated 40,000 persons die and another 40,000 experience long-term disability Figure. Phylogenetic analysis of HEV open reading frame 2 sequences isolated from Mytilus spp. RNA was isolated from 50–100 mg of digestive gland or gill. Tissue was as a result of consuming raw or homogenized in 300 μL phosphate-buffered saline, and viral RNA was isolated by using a undercooked shellfi sh (10). This study, viral RNA kit (QIAGEN, Crawley, UK), and PCR was conducted by amplifying nucleotides demonstrating the presence of HEV in 6332–6476 as described (8). The nucleotide sequences were aligned and bootstrapped, mussels collected locally in Scotland and phylogenetic neighbor-joining trees were constructed by using the ClustalW software for human consumption, raises (www.ebi.ac.uk/Tools/msa/clustalw2/). Phylogenetic trees were visualized by using FigTree (http://tree.bio.ed.ac.uk/software/fi gtree/). Bootstrap values >70% are indicated. Scale concern as to whether these shellfi sh bar indicates nucleotide substitutions per site. Sample site codes: AB, Ardrossan Beach; are a potential source of infection, as LB, Lunderston Bay; ABN, Aberdeen; FB, Ferrybridge; YE, Ythan Estuary. Sequences: reported (2). The association between Sw, swine; hu, human (followed by country of origin). GenBank accession numbers for environmental contamination with reference sequences: HEV genotype 1, B73218; HEV genotype 2, M74506; HEV genotype HEV and possible transmission by 3, CO31008; HEV genotype 4, C272108; huUK (KernowC1), HQ389543; HuUS, JN837481; swUK AF503512; huFrance, JN906974; swCanada, AY115488; swSpain, JQ522948; eating shellfi sh warrants investigation. sw2Japan AB248521, huJapan AB161719.

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This work was supported by 8. Erker JC, Desai SM, Mushahwar IK. sp.) that had just been caught. He European Commission FP6 funded project Rapid detection of hepatitis E virus RNA reported no history of traveling to a by reverse transcription–polymerase chain LSHB-CT-2006-037377 and by the Chief reaction using universal oligonucleotide gnathostomiasis-endemic area. Initial Scientist Offi ce Scotland project reference primers. J Virol Methods. 1999;81:109– work-up depicted eosinophilia (43%), ETM/32. 13. http://dx.doi.org/10.1016/S0166-0934 and a computed tomographic scan of (99)00052-X the chest revealed left pleural effusion. 9. Li TC, Miyamura T, Takeda N. Detection Claire Crossan, Paul J. Baker, of hepatitis E virus RNA from the bivalve Two weeks later, winding, linear, John Craft, Yasu Takeuchi, Yamato-Shijimi (Corbicula japonica) in reddish lesions appeared on his back, Harry R. Dalton, Japan. Am J Trop Med Hyg. 2007;76:170– which lasted 3 days (Figure, panel 2. A). Serologic testing for Schistosoma and Linda Scobie 10. Shuval H. Estimating the global burden of Author affi liations: Glasgow Caledonian thalassogenic diseases: human infectious mansoni was weakly positive. Acute University, Glasgow, Scotland, UK (C. diseases caused by wastewater pollution schistosomiasis was diagnosed, and of the marine environment. J Water Crossan, P.J. Baker, J. Craft, L. Scobie); treatment with praziquantel was Health. 2003;1:53–64. University College London, London, UK begun. In 4 weeks, all symptoms faded. (Y. Takeuchi); and European Centre for Address for correspondence: Linda Scobie, In 2009, the patient took Environment and Human Health, University Department of Life Sciences, Glasgow albendazol for helminthic of Exeter Medical School, Truro, UK (H.R. Caledonian University, Cowcaddens Rd, prophylaxis, and 3 weeks later, deep Dalton) Glasgow, G4 0BA, UK; email: linda.scobie@ migratory, swelling, reddish nodules gcu.ac.uk DOI: http://dx.doi.org/10.3201/eid1812.120924 occurred on the thorax; each lesion lasted ≈6 days, and new lesions References appeared at intervals of 1–5 days 1. Kamar N, Bendall R, Legrand-Abravanel in a somewhat linear array (Figure, F, Xia NS, Ijaz S, Izopet J, et al. Hepatitis E. panel B). By this time, hemograms Lancet. 2012;379:2477–88. http://dx.doi. displayed eosinophilia of 25%, but org/10.1016/S0140-6736(11)61849-7 a computed tomographic scan of 2. Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, et al. Hepatitis E Autochthonous the chest showed no abnormalities. outbreak on cruise ship. Emerg Infect Results of a complete ophthalmologic Dis. 2009;15:1738–44. http://dx.doi. Gnathostomiasis, examination were unremarkable, and org/10.3201/eid1511.091094 Brazil a fecal examination was negative 3. McCreary C, Martelli F, Grierson S, for parasites. Gnathostomiasis Ostanello F, Nevel A, Banks M. Excretion To the Editor: Gnathostomiasis of hepatitis E virus by pigs of different was highly suspected on the basis is an infestation by nematodes of ages and its presence in slurry stores in the of the clinical and epidemiologic the genus Gnathostoma; the main United Kingdom. Vet Rec. 2008;163:261– fi ndings and results of skin biopsies. 5. http://dx.doi.org/10.1136/vr.163.9.261 source of infection is raw freshwater Histopathologic examination re- 4. Emerson SU, Arankalle VA, Purcell RH. fi sh. In the past, gnathostomiasis was Thermal stability of hepatitis E virus. J vealed a dense superfi cial and deep regarded as restricted to certain Asian Infect Dis. 2005;192:930–3. http://dx.doi. dermal infi ltrate of eosinophils and and Central American countries, but org/10.1086/432488 neutrophils but did not show the 5. Lowther JA, Gustar NE, Powell AL, increase of migratory fl ux and changes parasite. Two samples of plasma were Hartnell RE, Lees DN. A two-year in alimentary habits have contributed systematic study to assess norovirus sent to Thailand for immunoblot in to importing cases into areas where contamination in oysters from commercial search of the diagnostic band (24-kDa the disease is not endemic (1,2). harvesting areas in the United Kingdom. antigen) of Gnathostoma spinigerum, Appl Environ Microbiol. 2012;78:5812–7. We report a case of autochthonous resulting in high titers. Albendazol, 6. Baker K, Morris J, McCarthy N, Saldana gnasthostomiasis in Brazil. L, Lowther J, Collinson A, et al. An 800 mg/day for 21 days, and a A 37-year-old man from Rio de outbreak of norovirus infection linked to single dose of ivermectin, 0.2 mg/ Janeiro sought medical attention in oyster consumption at a UK restaurant, kg, were administered and, despite February 2010. J Public Health (Oxf). 2005 because of low fever, cough, initial improvement, the disease 2011;33:205–11. abdominal tenderness, and pain in 7. McLeod C, Hay B, Grant C, Greening G, relapsed, requiring a second cycle of the left shoulder. The symptoms Day D. Inactivation and elimination of the medications. No signs of disease started 15 days after a recreational human enteric viruses by Pacifi c oysters. occurred during 2 years of follow-up. J Appl Microbiol. 2009;107:1809–18. trip to Tocantins, where he practiced Gnathostomiasis is found http://dx.doi.org/10.1111/j.1365- sport fi shing and ate sashimi- 2672.2009.04373.x mostly in Japan and Thailand. In the style freshwater raw fi sh (Cichla Americas, most cases occur in Mexico

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