Outbreak of Influenza A(H7N2) Among Cats in an Animal Shelter With Cat-to-Human Transmission—New York City, 2016

Abstract

We describe the first case of cat-to-human transmission of influenza A(H7N2), an avian-lineage influenza A virus, that occurred during an outbreak among cats in New York City animal shelters. We describe the public health response and investigation.

avian influenza, novel influenza, zoonotic infection

Influenza A(H7N2), a low pathogenic avian-lineage influenza virus, circulated in live poultry markets in the eastern and northeastern United States during 1994–2006 [1, 2] and caused outbreaks among poultry in Pennsylvania during 1997−1998 and 2001−2002, and in Virginia, West Virginia, and North Carolina in 2002 [3]. Two previously documented US human infections have occurred with this North American H7N2 lineage [4]: 1 serologically confirmed infection in a person culling an infected flock during the 2002 Virginia outbreak [5], and a second infection in an immunocompromised patient in New York in 2003 with no known poultry exposure [6]. The North American lineage A(H7N2) virus has not been detected widely by surveillance in poultry farms or live bird markets in the United States since 2006 [2]. Avian influenza virus infections in cats have rarely been documented [7–9]; no cat has ever been documented to have an A(H7N2) infection or to transmit an influenza virus to a human.

On 14 December 2016, the New York City Department of Health and Mental Hygiene (NYC DOHMH) was notified of a cat admitted to a Manhattan shelter on 12 November that died on 25 November and was confirmed positive for influenza A(H7N2) virus [10]. Subsequent testing of oropharyngeal aspirates of animals in the same shelter by the University of Wisconsin identified widespread infection with influenza A(H7N2) virus among cats, but no evidence of infection among dogs, chickens, or rabbits. We conducted case finding to detect human infections from cat-to-human transmission and implemented measures to reduce the risk for transmission to humans and cats.

PUBLIC HEALTH INVESTIGATION

We conducted case finding among persons who had adopted cats from, or were employed by or volunteered at the Manhattan shelter during 12 November–29 December 2016. A suspected case was defined as conjunctivitis (a previously described manifestation of human A(H7N2) virus infection [4, 11]) or ≥2 symptoms of sore throat, fever, muscle aches, or cough, with onset ≤10 days after exposure to a cat from the shelter.

During 15–21 December 2016, 188 of 385 persons who had adopted a cat from the shelter were reachable and agreed to an interview. Ten (5.3%) reported illness meeting the suspected case definition; 7 were assessed by medical epidemiologists to either have low risk for exposure (eg, symptom onset before date of adoption) or a specimen unlikely to test positive for influenza A(H7N2) (eg, symptom onset >30 days before interview), and were not tested. The remaining 3 persons who reported illness meeting the suspected case definition were tested for presence of influenza A RNA by real-time reverse-transcription polymerase chain reaction (rRT-PCR) at the NYC Public Health Laboratory (PHL) using primers, probes, and protocols from the Centers for Disease Control and Prevention (CDC). Influenza A RNA was not detected in any specimen.

During 16–18 December, NYC DOHMH opened and operated a temporary clinic site to interview and test all shelter employees and volunteers who had worked with cats at the shelter (n = 265); unvaccinated persons were offered seasonal influenza vaccine, and persons with illness meeting the suspected case definition were offered oseltamivir. A total of 165 (62.3%) employees and volunteers were interviewed and had nasopharyngeal specimens collected and tested regardless of presence of symptoms. A total of 24 (14.5%) had illness that met the suspected case definition. Seasonal influenza A(H3N2) virus RNA was detected in a sample from 1 symptomatic person; influenza A virus RNA was not detected in any other specimen.

On 19 December, NYC DOHMH was notified of an ill veterinarian who was not a regular employee or volunteer at the Manhattan shelter but who had obtained deep oropharyngeal aspirates from symptomatic cats at the Manhattan shelter to test for influenza virus during the previous week. This activity resulted in prolonged exposure, without a mask, respirator, or face shield, to respiratory secretions of cats infected with A(H7N2). Illness onset date was 18 December, the same day that the patient traveled by commercial airline. The patient reported a mild illness, characterized by sore throat, myalgia, and cough. On 19 December, NYC DOHMH interviewed the patient and collected a nasopharyngeal specimen, from which influenza A virus RNA, unsubtypeable as H3 or H1, was detected by rRT-PCR at NYC PHL. Influenza A virus RNA was not detected from a repeat nasopharyngeal specimen collected the following day. The patient was treated with oseltamivir and symptoms resolved without hospitalization.

The CDC performed genetic sequencing from the specimen collected on 19 December and an embryonated chicken egg–isolated virus and confirmed influenza A(H7N2) virus infection. The virus (A/New York/108/2016 [H7N2]) sequence (Global Initiative on Sharing All Influenza Data (GISAID): EPI944622-EPI944629) was nearly identical to the virus isolated from the infected cat, which had been sequenced by the US Department of Agriculture (USDA) National Veterinary Services Laboratories and the University of Wisconsin Veterinary Diagnostic Laboratory. Analysis of viruses isolated from the human and cat revealed that they were North American lineage low pathogenic avian influenza A(H7N2) viruses and were similar to H7N2 viruses that circulated and evolved in live bird markets in the eastern and northeastern United States during the early 2000s and resulted in 2 human infections in 2002 and 2003.

We conducted contact tracing of persons who had prolonged, close contact to the person with the confirmed case to determine whether human-to-human transmission had occurred. Five persons had close contact with the patient during 17 December–20 December 2016 (1 day before symptom onset until the day of the negative nasopharyngeal specimen). Of these, 4 were interviewed, and none developed symptoms ≤10 days after last exposure to the patient. Health departments attempted to contact 26 airline passengers who sat near the patient and 4 flight attendants, of whom 20 were contacted; none reported developing influenza-like symptoms ≤10 days after the flight. No additional cases of H7N2 influenza in humans were identified.

PUBLIC HEALTH MEASURES

On 15 December, representatives from the USDA, the New York State Department of Agriculture and Markets, and NYC DOHMH assessed entrance and exit procedures, employee clothing changes, and personal protective equipment (PPE) use at the Manhattan shelter. Staff from NYC DOHMH trained shelter staff on the correct use of gowns, gloves, shoe covers, and face shields when handling ill or exposed cats. In addition, use of fit-tested N95 respirators was recommended for persons collecting respiratory specimens from ill or exposed cats.

Further testing of cats identified feline A(H7N2) infection at 2 other NYC-operated shelters that had received cats from the Manhattan shelter. On 15 December, all 3 shelters ceased adoptions and movement of cats between shelters and limited intakes of new cats. On 29 December, the American Society for the Prevention of Cruelty to Animals and partners established a temporary biosecure shelter to allow affected shelters to disinfect and resume normal operations and to provide a contained space to care for >500 ill or exposed cats. The temporary facility was closed on 14 March 2017, after repeat oropharyngeal testing indicated that viral shedding had ended. Residents from >30 states volunteered at the facility; NYC DOHMH provided weekly line lists of volunteers and protocols to their respective health departments in case these persons developed influenza-like illness after returning home from NYC, and ≤10 days from their last exposure to the facility. No additional human infections were reported.

DISCUSSION

This is the first documented cat-to-human transmission of influenza A virus infection, which occurred during an influenza A(H7N2) outbreak among cats. Cat-to-human transmission of influenza A viruses is concerning because cats are companion animals and have close contact with humans. We identified only 1 case of human A(H7N2) virus infection that occurred after prolonged and unprotected exposure to ill cats and their respiratory secretions, which indicates that risk for cat-to-human transmission was low. Because case finding among humans was initiated >1 month after the index cat entered the shelter, earlier infections among persons who adopted or worked with cats might have been missed. We found no evidence of human-to-human transmission, supporting laboratory evidence of limited transmission of A(H7N2) among co-housed ferrets [12].

The outbreak among cats in NYC raises important questions about the reemergence of this influenza virus in the United States. It is unclear whether A(H7N2) virus was circulating among cats or other species before this outbreak. The detection of A(H7N2) virus infections in other shelters likely resulted from the movement of cats among shelters. Because cats are not routinely tested for influenza viruses, efforts to determine serologic prevalence of H7N2 infection among community-dwelling cats in NYC and other jurisdictions are needed to determine the extent of H7N2 virus transmission among cats.

NYC DOHMH activated its Incident Command System to provide surge staff capacity to rapidly determine whether there was any risk posed to humans by the outbreak among cats, which informed public messaging to persons who had adopted potentially infected cats and PPE requirements for persons working with infected cats. This outbreak highlights the importance of strong existing One Health partnerships between public health and animal health specialists at the local, state, and federal levels to allow for rapid and coordinated outbreak responses, particularly for novel influenza strains.

Notes

Disclaimer. The contents of this work are solely the responsibility of the authors and do not necessarily represent the official views of the Centers for Disease Control and Prevention (CDC).

Financial support. This work was supported by the Public Health Emergency Preparedness Cooperative Agreement (number NU90TP000546) and the Epidemiology and Laboratory Capacity for Infectious Diseases Cooperative Agreement (number NU50CK000407-03) from the CDC.

Potential conflicts of interest. All authors: No reported conflicts of interest. All authors have 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.

Influenza A(H7N2) Response Team

Bisrat Abraham, Joel Ackelsberg, Mike Antwi, Sharon Balter, Alexander Davidson, Paula Del Rosso, Katelynn Devinney, Marie Dorsinville, Anne Fine, Bruce Gutelius, Lucretia Jones, Ellen Lee, Kristen Lee, Natasha McIntosh, Nana Mensah, Sam Miller, Linda Moskin, Linda Ng, Stephanie Ngai, Beth Nivin, Carolyn Olson, Marc Paladini, Hilary Parton, Carolina Pichardo, Michael Porter, Ingrid Ramlakhan, Andrew Schroeder, David Starr, Norma Torres, Don Weiss, and Emily Westheimer (NYC DOHMH); Rebecca Hall and Tina Obijo (Division of Global Migration and Quarantine, CDC); Stephen Lindstrom and Atanaska Marinova-Petkova (Influenza Division, CDC); Kathy Toohey-Kurth (University of Wisconsin School of Veterinary Medicine); Mia Torchetti (Animal and Plant Health Inspection Service, US Department of Agriculture); Risa Weinstock (NYC Animal Care Centers).

Author notes

a

Members of the Influenza A(H7N2) Response Team are listed after the References.