Live Animal Markets in Minnesota: A Potential Source for Emergence of Novel Influenza A Viruses and Interspecies Transmission.

Mary J Choi1 Montserrat Torremorell2 Jeff B Bender2 Kirk Smith3 David Boxrud3 Jon R Ertl2 My Yang2 Kamol Suwannakarn2 Duachi Her3 Jennifer Nguyen3 Timothy M Uyeki1 Min Levine1 Stephen Lindstrom1 Jacqueline M Katz1 Michael Jhung1 Sara Vetter3 Karen K Wong1 Srinand Sreevatsan2 Ruth Lynfield3
Affiliations 3 institutions
  1. Centers for Disease Control and Prevention, Atlanta, Georgia.
  2. University of Minnesota College of Veterinary Medicine, Minnesota Center of Excellence for Influenza Research and Surveillance.
  3. Minnesota Department of Health, St Paul.

Abstract

Live animal markets have been implicated in transmission of influenza A viruses (IAVs) from animals to people. We sought to characterize IAVs at 2 live animal markets in Minnesota to assess potential routes of occupational exposure and risk for interspecies transmission. We implemented surveillance for IAVs among employees, swine, and environment (air and surfaces) during a 12-week period (October 2012-January 2013) at 2 markets epidemiologically associated with persons with swine-origin IAV (variant) infections. Real-time reverse transcription polymerase chain reaction (rRT-PCR), viral culture, and whole-genome sequencing were performed on respiratory and environmental specimens, and serology on sera from employees at beginning and end of surveillance. Nasal swabs from 11 of 17 (65%) employees tested positive for IAVs by rRT-PCR; 7 employees tested positive on multiple occasions and 1 employee reported influenza-like illness. Eleven of 15 (73%) employees had baseline hemagglutination inhibition antibody titers ≥40 to swine-origin IAVs, but only 1 demonstrated a 4-fold titer increase to both swine-origin and pandemic A/Mexico/4108/2009 IAVs. IAVs were isolated from swine (72/84), air (30/45), and pen railings (5/21). Whole-genome sequencing of 122 IAVs isolated from swine and environmental specimens revealed multiple strains and subtype codetections. Multiple gene segment exchanges among and within subtypes were observed, resulting in new genetic constellations and reassortant viruses. Genetic sequence similarities of 99%-100% among IAVs of 1 market customer and swine indicated interspecies transmission. At markets where swine and persons are in close contact, swine-origin IAVs are prevalent and potentially provide conditions for novel IAV emergence.

Supporting text Virus Host Location
human 14 influenza 61 live animal markets 2 swine 267 Marketing 1 Occupational Exposure 10 Animals 1948 Antibodies, Viral 212 Environmental Microbiology 4 Epidemiological Monitoring 27 Humans 1440 Influenza A virus 186 Minnesota 2 Orthomyxoviridae Infections 228 Prospective Studies 7 Real-Time Polymerase Chain Reaction 18 Sequence Analysis, DNA 113 Swine 258 Swine Diseases 153 Virus Cultivation 10 Zoonoses 397

Evidence records

9 total
Zoonotic Surveillance
7 records · 4 evidence types
Evidence type
3 records
OVE2153
Key finding

Influenza A viruses were successfully isolated from swine at live animal markets in Minnesota.

Virus
Host
Location
Not specified
Supporting text

IAVs were isolated from swine (72/84), air (30/45), and pen railings (5/21).

Sample type
swine specimens
OVE2154
Key finding

Influenza A viruses were successfully isolated from air samples collected at live animal markets.

Virus
Host
Not specified
Location
Not specified
Supporting text

IAVs were isolated from swine (72/84), air (30/45), and pen railings (5/21).

Sample type
air samples
OVE2155
Key finding

Influenza A viruses were successfully isolated from pen railing surface samples in live animal markets.

Virus
Host
Not specified
Location
Not specified
Supporting text

IAVs were isolated from swine (72/84), air (30/45), and pen railings (5/21).

Sample type
surface samples from pen railings
Evidence type
1 records
OVE2150
Key finding

Influenza A viruses were detected by rRT-PCR in nasal swabs from live animal market employees in Minnesota.

Virus
Host
Location
Supporting text

We sought to characterize IAVs at 2 live animal markets in Minnesota to assess potential routes of occupational exposure and risk for interspecies transmission. Nasal swabs from 11 of 17 (65%) employees tested positive for IAVs by rRT-PCR.

Method
rRT-PCR | real-time reverse transcription polymerase chain reaction
Sample type
Nasal swabs
Geographic raw
Minnesota
Country inferred
USA
Evidence type
2 records
OVE2151
Key finding

Eleven of fifteen employees showed baseline hemagglutination inhibition antibody titers ≥40 to swine-origin influenza A viruses, indicating prior exposure.

Virus
Host
Location
Not specified
Supporting text

Eleven of 15 (73%) employees had baseline hemagglutination inhibition antibody titers ≥40 to swine-origin IAVs.

Method
hemagglutination inhibition assay
Sample type
sera
OVE2152
Key finding

One employee demonstrated a four-fold titer increase to both swine-origin and pandemic A/Mexico/4108/2009 influenza A viruses, consistent with seroconversion during surveillance.

Virus
Host
Location
Not specified
Supporting text

Eleven of 15 (73%) employees had baseline hemagglutination inhibition antibody titers ≥40 to swine-origin IAVs, but only 1 demonstrated a 4-fold titer increase to both swine-origin and pandemic A/Mexico/4108/2009 IAVs.

Method
hemagglutination inhibition assay
Sample type
sera
Evidence type
1 records
OVE2158
Key finding

Swine-origin IAVs were prevalent at live animal markets in Minnesota where swine and humans were in close contact, creating conditions for novel IAV emergence.

Virus
Host
Location
Supporting text

Live Animal Markets in Minnesota: A Potential Source for Emergence of Novel Influenza A Viruses and Interspecies Transmission. At markets where swine and persons are in close contact, swine-origin IAVs are prevalent and potentially provide conditions for novel IAV emergence.

Method
surveillance | real-time reverse transcription polymerase chain reaction (rRT-PCR) | viral culture | whole-genome sequencing | serology
Sample type
nasal swabs | air | pen railings | respiratory specimens | environmental specimens
Geographic raw
Minnesota
Country inferred
USA
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE2157
Key finding

IAVs from a market customer and swine showed 99%-100% genetic sequence similarity, indicating interspecies transmission.

Virus
Host
Location
Not specified
Supporting text

Genetic sequence similarities of 99%-100% among IAVs of 1 market customer and swine indicated interspecies transmission.

Method
whole-genome sequencing | genetic similarity analysis
Study design
market-based surveillance study
Transmission direction
animal-to-human
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE2156
Key finding

Whole-genome sequencing identified reassortant influenza A viruses with new genetic constellations generated by gene segment exchanges among and within subtypes.

Virus
Host
Not specified
Location
Not specified
Supporting text

Multiple gene segment exchanges among and within subtypes were observed, resulting in new genetic constellations and reassortant viruses.

Event type
reassortment
Genes or segments
gene segments