OmniVira

Evidence for Cross-species Influenza A Virus Transmission Within Swine Farms, China: A One Health, Prospective Cohort Study.

Mai-Juan Ma1 Guo-Lin Wang1 Benjamin D Anderson2 Zhen-Qiang Bi3,4 Bing Lu5 Xian-Jun Wang3,4 Chuang-Xin Wang6 Shan-Hui Chen5 Yan-Hua Qian5 Shao-Xia Song3,4 Min Li6 John A Lednicky7 Teng Zhao1 Meng-Na Wu1 Wu-Chun Cao1 Gregory C Gray2,8,9
Affiliations 9 institutions
  1. State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, China.
  2. Global Health Institute, Division of Infectious Diseases, School of Medicine, Duke University, Durham, North Carolina.
  3. Shandong Provincial Center for Disease Control and Prevention.
  4. Shandong Provincial Key Laboratory of Disease Control and Prevention, Jinan.
  5. Wuxi Center for Disease Control and Prevention, Wuxi.
  6. Licheng District Center for Disease Control and Prevention, Jinan, China.
  7. Department of Environmental and Global Health, College of Public Health and Health Professions, University of Florida, Gainesville.
  8. Global Health Research Center, Duke Kunshan University, Kunshan, China.
  9. Program in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore.
PMID29401271 DOI10.1093/cid/cix823 Year2018 Journal Clinical infectious diseases : an official publication of the Infectious Diseases Society of America Clin Infect Dis Languageeng Statusppublish

Abstract

Our understanding of influenza A virus transmission between humans and pigs is limited. Beginning in 2015, we used a One Health approach and serial sampling to prospectively study 299 swine workers and 100 controls, their 9000 pigs, and 6 pig farm environments in China for influenza A viruses (IAVs) using molecular, culture, and immunological techniques. Study participants were closely monitored for influenza-like illness (ILI) events. Upon enrollment, swine workers had higher serum neutralizing antibody titers against swine H1N1 and higher nasal wash total immunoglobulin A (IgA) and specific IgA titers against swine H1N1 and H3N2 viruses. Over a period of 12 months, IAVs were detected by quantitative reverse-transcription polymerase chain reaction in 46 of 396 (11.6%) environmental swabs, 235 of 3300 (7.1%) pig oral secretion, 23 of 396 (5.8%) water, 20 of 396 (5.1%) aerosol, and 19 of 396 (4.8%) fecal-slurry specimens. Five of 32 (15.6%) participants with ILI events had nasopharyngeal swab specimens that were positive for IAV, and 17 (53.1%) demonstrated 4-fold rises in neutralization titers against a swine virus. Reassorted Eurasian avian-lineage H1N1, A(H1N1)pdm09-like, and swine-lineage H3N2 viruses were identified in pig farms. The A(H1N1)pdm09-like H1N1 viruses identified in swine were nearly genetically identical to the human H1N1 viruses isolated from the participants with ILI. There was considerable evidence of A(H1N1)pdm09-like, swine-lineage H1N1, and swine-lineage H3N2 viruses circulating, likely reassorting, and likely crossing species within the pig farms. These data suggest that stronger surveillance for novel influenza virus emergence within swine farms is imperative.

Supporting text Virus Host Location
China 230 emerging pathogens 3 influenza A virus 227 One Health 98 swine 267 Adolescent 34 Adult 71 Aged 31 Animals 1948 Antibodies, Neutralizing 80 Antibodies, Viral 212 Farmers 5 Farms 30 Female 289 Humans 1440 Immunity, Mucosal 2 Influenza A Virus, H1N1 Subtype 74 Influenza A Virus, H3N2 Subtype 48 Influenza, Human 286 Male 224 Middle Aged 60 One Health 14 Orthomyxoviridae Infections 228 Prospective Studies 7

Evidence records

7 total
Zoonotic Surveillance
5 records · 3 evidence types
Evidence type Virus Isolation
1 records
OVE2863 Virus Isolation
Key finding

Human H1N1 viruses were isolated from participants with influenza-like illness in the China swine farm cohort.

Virus
Influenza A virus H1N1
Host
human Homo sapiens Natural host
Location
Not specified
Supporting text

The A(H1N1)pdm09-like H1N1 viruses identified in swine were nearly genetically identical to the human H1N1 viruses isolated from the participants with ILI.

Sample type
nasopharyngeal swab
Evidence type Viral Detection
1 records
OVE2860 Viral Detection
Key finding

Influenza A viruses were detected by qRT-PCR in multiple sample types from pigs and farm environments in China.

Virus
Influenza A virus
Host
pig Sus scrofa Natural host
Location
China
Supporting text

Beginning in 2015, we used a One Health approach and serial sampling to prospectively study 299 swine workers and 100 controls, their 9000 pigs, and 6 pig farm environments in China for influenza A viruses (IAVs) using molecular, culture, and immunological techniques. Over a period of 12 months, IAVs were detected by quantitative reverse-transcription polymerase chain reaction in 46 of 396 (11.6%) environmental swabs, 235 of 3300 (7.1%) pig oral secretion, 23 of 396 (5.8%) water, 20 of 396 (5.1%) aerosol, and 19 of 396 (4.8%) fecal-slurry specimens.

Method
quantitative reverse-transcription polymerase chain reaction (qRT-PCR)
Sample type
environmental swabs | pig oral secretion | water | aerosol | fecal-slurry specimens
Geographic raw
China
Country inferred
CHN
Evidence type Serological Evidence
3 records
OVE2857 Serological Evidence
Key finding

Swine workers showed higher serum neutralizing antibody titers and specific IgA titers against swine H1N1 compared to controls.

Virus
Influenza A virus H1N1
Host
human Homo sapiens Natural host
Location
Not specified
Supporting text

Upon enrollment, swine workers had higher serum neutralizing antibody titers against swine H1N1 and higher nasal wash total immunoglobulin A (IgA) and specific IgA titers against swine H1N1 and H3N2 viruses.

Method
neutralizing antibody assay | immunoglobulin A (IgA) assay
Sample type
serum | nasal wash
OVE2859 Serological Evidence
Key finding

Seventeen of thirty-two participants with influenza-like illness showed fourfold rises in neutralization titers against a swine virus.

Virus
swine virus
Host
human Homo sapiens Natural host
Location
Not specified
Supporting text

Five of 32 (15.6%) participants with ILI events had nasopharyngeal swab specimens that were positive for IAV, and 17 (53.1%) demonstrated 4-fold rises in neutralization titers against a swine virus.

Method
neutralization assay
Sample type
serum
OVE2858 Serological Evidence
Key finding

Swine workers had higher nasal wash specific IgA titers against swine H3N2 viruses than controls.

Virus
Influenza A virus H3N2
Host
human Homo sapiens Natural host
Location
Not specified
Supporting text

Upon enrollment, swine workers had higher serum neutralizing antibody titers against swine H1N1 and higher nasal wash total immunoglobulin A (IgA) and specific IgA titers against swine H1N1 and H3N2 viruses.

Method
immunoglobulin A (IgA) assay
Sample type
nasal wash
Transmission Evidence
1 records · 1 evidence types
Evidence type Cross-species Transmission
1 records
OVE2862 Cross-species Transmission
Key finding

A(H1N1)pdm09-like H1N1 viruses detected in swine were nearly genetically identical to human H1N1 viruses isolated from participants with influenza-like illness, indicating cross-species influenza A virus transmission within swine farms in China.

Virus
Influenza A virus H1N1
Host
human Homo sapiens Natural host pig Sus scrofa Natural host
Location
China
Supporting text

Reassorted Eurasian avian-lineage H1N1, A(H1N1)pdm09-like, and swine-lineage H3N2 viruses were identified in pig farms. The A(H1N1)pdm09-like H1N1 viruses identified in swine were nearly genetically identical to the human H1N1 viruses isolated from the participants with ILI.

Method
genomic sequencing | isolation | molecular detection
Study design
prospective cohort study with genomic comparison
Transmission direction
cross-species transmission
Geographic raw
pig farms, China
Genomic Evolution
1 records · 1 evidence types
Evidence type Recombination or Reassortment
1 records
OVE2861 Recombination or Reassortment
Key finding

Reassorted Eurasian avian-lineage H1N1, A(H1N1)pdm09-like, and swine-lineage H3N2 influenza A viruses were identified from pigs on farms in China.

Virus
Influenza A virus H1N1 Influenza A virus H3N2
Host
Not specified
Location
Not specified
Supporting text

Reassorted Eurasian avian-lineage H1N1, A(H1N1)pdm09-like, and swine-lineage H3N2 viruses were identified in pig farms.

Event type
reassortment