Editorial Commentary: This Little Piggy Went to Market—but Perhaps Should Have Stayed Home

Clinical Infectious Diseases, Oct 2015

Richard J. Webby

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Editorial Commentary: This Little Piggy Went to Market—but Perhaps Should Have Stayed Home

CID This Little Piggy Went to Market-but Perhaps Should Have Stayed Home Richard J. Webby 0 0 Department of Infectious Diseases, St Jude Children's Research Hospital , Memphis, Tennessee EDITORIAL COMMENTARY influenza; zoonotic; animal markets - Influenza A is a zoonotic disease. Although some causative viruses have become adapted to humans and circulate exclusively in this host, the animal reservoirs are the source of all past and future pandemic strains. With this knowledge, there has been decades of research toward identifying the interfaces where infected animals and humans are most likely to interact. A particular target of these studies has been live bird markets, particularly in Asia. While the importance of these markets had been previously recognized [1], the H5N1 outbreak in Hong Kong in 1997, where 6 of 18 persons known to be infected with the virus died, refocused much of influenza’s public health attention [2]. Live bird markets provide a prime environment to support the evolution of influenza A viruses and promote human infection. Not only are different hosts of influenza—including humans— each with their own variants of the virus, brought together in unnatural proximity, but as fresh animals are introduced to replenish stocks, new susceptible hosts are made available, allowing the virus to spread and be maintained for prolonged periods. The importance of live bird markets in the ecology of influenza was again highlighted in 2013 when human H7N9 infections were detected in China [3]. The correlation between the closing of the market systems and the drop-off in human cases suggested markets as the likely source of infection. Although mammalian species have been present in some of the markets studied, the majority of influenza work has centered on the role of the avian species. In this issue of Clinical Infectious Diseases, Choi and colleagues have provided convincing evidence that animal markets that sell swine present another active interface in which infected animals and humans interact and where zoonotic infections occur [4]. Surprising to many will be the fact that these markets are located not in Asia, but in the United States. In what is a textbook example of collaboration between academia and veterinary and public health, this team of investigators undertook a 12-week surveillance program in 2 mixed-species markets in the state of Minnesota targeting swine, environmental surfaces, and employees. The 2 markets were selected based on epidemiologic evidence that suggested them as possible sources for prior zoonotic influenza infections. Although a number of interesting observations were made and detailed in the manuscript, one striking finding was the surprisingly high level of influenza virus detected in market employees. Eleven of the 17 employees tested positive at least once for the presence of influenza virus RNA during the 12-week period. Although half of these positive samples were unsubtypable due to viral load issues, 4 were confirmed to be H3N2 viruses of swine origin, with the remaining 7 being seasonal H3N2 influenza viruses. The relatively high detection of H3N2 viruses of swine origin in the employees is a challenge to interpret. Real-time reverse transcription polymerase chain reaction (PCR) cycle threshold values were all high, and it is possible that detections represented true viral infection or, alternatively, fomite contamination of the nasal cavity. Influenza viruses were detected in pigs, air samples, pen railings, and other environmental surfaces in the markets, and there was a marked lack of clinical symptoms reported, indicating that the latter is a real possibility. Regardless, the fact that virus genetic material was detected in nasal cavities demonstrates ample exposure and, at minimum, a threat of infection. Unfortunately, the high degree of antigenic similarity between many of the swine and human influenza viruses circulating in the United States, and in many parts of the world, limits the usefulness of serology in interpreting the PCR results. Indeed, most of the employees had baseline serologic reactivity to the swine viruses, including 67% with immunity to the H3N2 swine viruses detected. This alone could account for the low levels of clinical symptoms reported. Somewhat fortuitously for the study, but not the patient, a 12-year-old boy developed respiratory illness 3 days after visiting one of the markets. Follow-up studies showed that he was infected with a virus with gene segments near-identical to those detected in swine in the same location, direct evidence of market-to-human transmission. Studies such as this one are not simple to conduct, with a number of professional, ethical, and trust issues to overcome. They are, however, critical to further our understanding of zoonotic influenza and the factors that favor it, and to fuel subsequent laboratory studies to identify the underlying virologic features of interspecies transmission. As such, the authors are to be congratulated on an important, invaluable, and well-conducted study. The amount of education, preparation, and consultation that went into this study must have been substantial. On another level, this study again brings into question the wisdom of live animal markets. There is ample evidence to support a human health threat from live birds in these markets, and now mammalian hosts as well. While there is a clear cultural demand for their products, there is also an undisputable risk. There is currently much discussion on influenzarelated laboratory biosafety issues. Markets such as the one described in this study represent a far greater threat; changes must be made to how they operate. Whether it is manipulations to airflow, animal husbandry, sanitary practices, or other novel solutions, studies to assess the impact of intervention strategies in real-world settings are needed. Since 1997, Hong Kong authorities have implemented a number of programs that have reduced the diversity and overall viral burden within their poultry markets (see, eg, [5]), providing proof that it can be done. In each case, these decisions were based on solid, but not necessarily highly fundable, scientific studies. The scope of the problem is large, but the hurdles not unsurmountable. Studies such as that by Choi et al are the perfect place to start. Note Potential conflict of interest. Author certifies no potential conflicts of interest. The author has submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. References 1. Senne D , Pearson JE , Panigrahy B. Live poultry markets: a missing link in the epidemiology of avian influenza . In: Proceedings of the Third International Symposium on Avian Influenza , US Animal Health Association , St Joseph , MO, 1992 : 50 - 8 . 2. Claas EC , Osterhaus AD , van Beek R , et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus . Lancet 1998 ; 351 : 472 - 7 . 3. Gao R , Cao B , Hu Y , et al. Human infection with a novel avian-origin influenza A (H7N9) virus . N Engl J Med 2013 ; 368 : 1888 - 97 . 4. Choi MJ , Torremorell M , Bender JB , et al. Live animal markets in minnesota: a potential source for emergence of novel influenza a viruses and interspecies transmission . Clin Infect Dis 2015 ; 61 : 1355 - 62 . 5. Kung NY , Guan Y , Perkins NR , et al. The impact of a monthly rest day on avian influenza virus isolation rates in retail live poultry markets in Hong Kong . Avian Dis 2003 ; 47 : 1037 - 41 .

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Richard J. Webby. Editorial Commentary: This Little Piggy Went to Market—but Perhaps Should Have Stayed Home, Clinical Infectious Diseases, 2015, 1363-1364, DOI: 10.1093/cid/civ620