The Pennsylvania State University The Graduate School College of Health and Human ...

182 Pages·2015·2.09 MB·English

by  Angela Spleen

The Pennsylvania State University
The Graduate School
College of Health and Human Development

A MULTISITE, PROSPECTIVE, ONE HEALTH INVESTIGATION OF ZOONOTIC SWINE INFLUENZA
AMONG 4-H MEMBERS AND THEIR SWINE AT AGRICULTURAL FAIRS IN PENNSYLVANIA

A Dissertation in Biobehavioral Health
by
Angela M. Spleen

©2015 Angela M. Spleen

Submitted in Partial Fulfillment
of the Requirements
for the Degree of

Doctor of Philosophy

August 2015
The dissertation of Angela M. Spleen was reviewed and approved* by the following:
Eugene J. Lengerich
Professor of Public Health Sciences and Biobehavioral Health
Dissertation Co-Adviser
Co-Chair of Committee

Linda A. Wray
Associate Professor of Biobehavioral Health
Dissertation Co-Adviser
Co-Chair of Committee

Frank M. Ahern
Senior Research Associate, Biobehavioral Health

Amanda Beaudoin
Infectious Disease Research Fellow, University of Minnesota Medical School
Special Member

Rachel A. Smith
Associate Professor of Communication Arts & Sciences and Human Development & Family
Studies

David R. Wolfgang
Field Studies Director, Co-Director Center for Animal Care and Health, Extension Veterinarian,
Veterinary and Biomedical Sciences
Special Member

Robert Turrisi
Professor of Biobehavioral Health and Prevention Research Center
Professor-in-Charge of the Graduate Program

*Signatures are on file in the Graduate School.
ABSTRACT
The unique animal-human interface created in an agricultural fair setting is a potential
hot-spot for transmission of zoonotic influenza. Swine have the ability to undergo infection
from swine, human, and avian influenza viruses, thus making them a likely source for emergent
influenza viruses capable of spreading in humans. Since 2005, 373 cases of variant influenza
(swine origin influenza virus that infects humans) have been reported in the United States.
Swine exhibitors, such as those from 4-H and their swine, may be responsible for outbreaks of
zoonotic influenza (e.g. H3N2v) at agricultural fairs. Although youth who exhibit swine at fairs
are recognized for their risk of contracting and/or introducing zoonotic influenza to the general
public, we know very little about their farm biosecurity risks or knowledge and behaviors
regarding zoonotic influenza.
A multi-site, prospective, One Health investigation that assessed interactions between
humans, animals, and the environment was conducted. This study used a convenience sample
of 138 4-H members and leaders of 4-H groups attending five county fairs in western, south-
central, and south-eastern Pennsylvania during the summer of 2014. The first aim of the
present study was to assess the incidence of influenza like illness in 4-H members and their
swine through fair and follow-up interviews and collection of nasal swab samples (human and
swine) and saliva samples (swine); swine samples were tested for influenza virus using RT-PCR
and virus isolation. The second aim was to quantify interrelated risk factors from multiple levels
including: fair environment, farm environment, and individual level knowledge and behaviors.
Observational assessments at each fair were used to characterize the fair environment.
Biosecurity risks for 4-H members were assessed in four domains: housing,
transportation/sharing, animal, and human through three surveys conducted prior to, during
and after the fair.
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No ILI or influenza virus was detected in humans or swine. Fair environment
assessments revealed that the availability of hand sanitization facilities and related
informational signage was poor across most fairs. Assessment of farm-level biosecurity risk in
the housing and transportation/sharing domains found that almost all participants’ swine
(91.3%) were kept on a farm with other types of livestock, 17% indicated they house their swine
on a farm with commercial livestock, and 16% transported their swine to other shows where
contact with other swine increases risk for influenza infection. Among the animal biosecurity
risk factors, poor quarantine procedures were indicated in 73% of respondents who traveled
to/exhibited at another event. As belief in biosecurity importance increased, the odds of
quarantining new or returning animals on the farm increased (OR:2.2; CI:1.0-4.8). Knowledge
summary scores from the human biosecurity domain were low, with the mean score below the
50% correct bench-mark. Approximately 27% of the participants did not know or did not believe
humans could contract disease from animals. 4-H members exhibited moderate risk in personal
protective equipment (PPE) use as evident by a mean PPE use score of 7.1 (range: 1-15; low-high
risk). For every one point increase in the knowledge summary score there was a 0.4 point (CI: -
0.7 - -0.05) decrease in the PPE risk score. 4-H member social networks did not appear to be
highly sex-assortative, but did assort by age and on average, participants who shared their tools
had much higher degree or number of connections than the participants who did not share their
tools.
While no ILI was detected, the fair environment lacked disease control measures. 4-H
members were largely unaware of zoonotic risk and their behaviors supported transmission of
variant swine influenza. We recommend the adoption of specific education and procedures to
reduce the potential for variant swine influenza outbreaks at agricultural fairs due to youth
swine exhibition.
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Table of Contents
List of Abbreviations ....................................................................................................................... vi
List of Tables ................................................................................................................................. viii
List of Figures .................................................................................................................................. ix
Acknowledgements.......................................................................................................................... x
CHAPTER 1: Introduction and Literature Review ............................................................................. 1
Introduction ................................................................................................................................. 1
Literature Review ......................................................................................................................... 2
Influenza Virus Biology ............................................................................................................. 4
Variant Swine Influenza ........................................................................................................... 6
Variant Swine Influenza at Agricultural Fairs ......................................................................... 11
Zoonotic Disease Related Knowledge & Biosecurity Practices .............................................. 14
4-H Youth Characteristics and Networks ............................................................................... 19
Chapter Two: Methodology ........................................................................................................... 23
Theoretical Framework .............................................................................................................. 23
Objective, Aims, and Research Questions ................................................................................. 26
Methods & Procedures .............................................................................................................. 31
Institutional Review Board Approval ..................................................................................... 31
Institutional Animal Care and Use Committee Approval ....................................................... 31
Study Design .......................................................................................................................... 31
Recruitment ........................................................................................................................... 32
Data Collection ....................................................................................................................... 33
Instrumentation ..................................................................................................................... 34
Analytic Strategy .................................................................................................................... 38
Chapter Three: County Agricultural Fair Environment and Farm Biosecurity Practices of 4-H
Swine Club Members in Pennsylvania, 2014 ................................................................................. 52
Introduction ............................................................................................................................... 52
Methods ..................................................................................................................................... 55
Results ........................................................................................................................................ 60
Discussion .................................................................................................................................. 63
Limitations ............................................................................................................................. 66
Conclusions ............................................................................................................................ 67
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Chapter Four: Zoonotic Disease-Related Knowledge and Behavior of 4-H Swine Club Members in
Pennsylvania, 2014 ........................................................................................................................ 74
Introduction ............................................................................................................................... 74
Methods ..................................................................................................................................... 76
Results ........................................................................................................................................ 80
Discussion .................................................................................................................................. 82
Limitations ............................................................................................................................. 85
Conclusions ............................................................................................................................ 86
Chapter Five: Activities and Social Networks of 4-H Swine Club Members at Four County
Agricultural Fairs in Pennsylvania, 2014 ........................................................................................ 93
Introduction ............................................................................................................................... 93
Methods ..................................................................................................................................... 97
Results ...................................................................................................................................... 101
Discussion ................................................................................................................................ 104
Limitations ........................................................................................................................... 106
Conclusions .......................................................................................................................... 106
Chapter Six: Discussion ................................................................................................................ 114
4-H Biosecurity Risks ................................................................................................................ 114
Fair Biosecurity Risks ................................................................................................................ 118
Interventions to Reduce Risk ................................................................................................... 119
Implications .............................................................................................................................. 122
Limitations & Future Studies ................................................................................................... 124
Conclusion ................................................................................................................................ 127
References ................................................................................................................................... 129
Appendix A: Primary Survey ........................................................................................................ 140
Appendix B: Extension Leader Interview Survey ......................................................................... 148
Appendix C: Fair Interview Survey ............................................................................................... 150
Appendix D: Follow-Up Interview Survey .................................................................................... 152
Appendix E: Observational Fair Environment Survey .................................................................. 154
Appendix F: Pilot Study Methods, Results and Recommendations ............................................. 155
Appendix G: Material and References for Survey Instrument Development .............................. 165

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List of Abbreviations
AMA: American Medical Association
APHIS: Animal and Plant Health Inspection Service
AVMA: American Veterinary Medical Association
CDC: Centers for Disease Control and Prevention
CI: Confidence Interval
DOH: Department of Health
EFA: Exploratory Factor Analysis
FAO: Food & Agricultural Organization
FFA: Future Farmers of America
GIP: Global Influenza Programme
GISRS: Global Influenza Surveillance Response System
HA: Hemagglutinin
HPAI: Highly Pathogenic Avian Influenza
IAV: Influenza A Virus
ILI: Influenza-Like Illness
MMWR: Morbidity and Mortality Weekly Report
NA: Neuraminidase
NASS: National Agricultural Statistics Service
NRC: National Research Council
OIE: World Organization for Animal Health
PA: Pennsylvania
PCR: Polymerase Chain Reaction
PPE: Personal Protective Equipment
SD: Standard Deviation
SE: Standard Error
SEM: Social Ecological Model
TIV: Trivalent Influenza Vaccine
UNICEF: United Nations Children’s Fund
UNSIC: United Nations System Influenza Coordination
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U.S.: United States
USDA: United States Department of Agriculture
UV: Ultraviolet
WHO: World Health Organization
vii
List of Tables
Table 1: Reported infections with variant influenza viruses in the United States since December
2005 ................................................................................................................................................. 8
Table 2: Detected United States human infections with H3N2v by state since August 2011 ......... 9
Table 3: Summary of 5 survey instruments used in Incidence, knowledge, and risk factors related
to zoonotic swine influenza among 4-H members and their swine .............................................. 36
Table 4: Transportation/sharing, housing, and animal biosecurity practices for 4-H swine club
members ........................................................................................................................................ 44
Table 5: Environmental biosecurity risk scores ranked from low to mid to high risk levels (1-3),
for 5 convenience sampled Pennsylvania agricultural fairs. .......................................................... 68
Table 6: Sociodemographic and farm characteristics for 4-H swine club members convenience
sampled from 5 counties in Pennsylvania ..................................................................................... 69
Table 7: Biosecurity behaviors for 4-H swine club members convenience sampled from 5
counties in Pennsylvania ................................................................................................................ 70
Table 8: Generalized linear model for factors associated with quarantine practices for 4-H swine
club members convenience sampled from 5 counties in Pennsylvania ........................................ 73
Table 9: Sociodemographic and personal health factors for 4-H swine club members from 5
convenience sampled Pennsylvania counties. ............................................................................... 87
Table 10: Infectious disease related knowledge and behavioral risk factors in 4-H members
from 5 convenience sampled Pennsylvania counties .................................................................. 88
Table 11: Generalized linear model for factors associated with PPE use in convenience sample 4-
H swine club members in Pennsylvania ......................................................................................... 91
Table 12: Generalized linear model for factors associated with hand-washing behaviors in
convenience sampled 4-H swine club members in Pennsylvania.................................................. 92
Table 13: Sociodemographic and fair activities of 4-H swine club members from 4 convenience
sampled Pennsylvania counties. .................................................................................................. 108
Table 14: Descriptive social network properties of friends, time spent, and shared tools
networks for 4-H swine club members from 4 convenience sampled Pennsylvania counties. .. 110
Table 15: Two-sample t-test for differences in mean degree centrality of 4-H members who
attend multiple shows versus 4-H members who attend one show ........................................... 111
viii
List of Figures
Figure 1: Social Ecological Model (SEM) of risk determinants for 4-H members who exhibit swine
at agricultural fairs. ........................................................................................................................ 24
Figure 2: Outline of research questions addressed in each manuscript (Chapters 3, 4, & 5) by
level of the SEM (Figure 1). ............................................................................................................ 30
Figure 3: Study schema for data collection. ................................................................................... 34
Figure 4: Photos exemplifying hand sanitization stations and signage regarding hand-sanitization
and disease transmission. .............................................................................................................. 40
Figure 5: Photos exemplifying high (left and middle) and moderate (right) risk levels for wash
stations. .......................................................................................................................................... 41
Figure 6: Domains for biosecurity risks. ......................................................................................... 42
Figure 7: County 1 networks of 4-H members self-reported tool sharing with nodes colored by
attending multiple shows or not (A), spent time with other 4-H swine club members at the fair
with nodes colored by attending multiple shows or not (B), and spent time 4-H swine club
members at the fair with nodes colored by age group (C). The node size on every graph is
proportional to the individuals’ degree and edge widths are proportional to the weighted value
of the relation (family ties have thicker lines). ............................................................................ 112
Figure 8: County 2 networks of 4-H members self-reported tool sharing with nodes colored by
attending multiple shows or not (A), spent time with other 4-H swine club members at the fair
with nodes colored by attending multiple shows or not (B), and spent time 4-H swine club
members at the fair with nodes colored by age group (C). The node size on every graph is
proportional to the individuals’ degree and edge widths are proportional to the weighted value
of the relation (family ties have thicker lines). ............................................................................ 112
Figure 9: County 3 networks of 4-H members self-reported tool sharing with nodes colored by
attending multiple shows or not (A), spent time with other 4-H swine club members at the fair
with nodes colored by attending multiple shows or not (B), and spent time 4-H swine club
members at the fair with nodes colored by age group (C). The node size on every graph is
proportional to the individuals’ degree and edge widths are proportional to the weighted value
of the relation (family ties have thicker lines). ............................................................................ 113
Figure 10: County 5 networks of 4-H members self-reported tool sharing with nodes colored by
attending multiple shows or not (A) and spent time 4-H swine club members at the fair with
nodes colored by age group (B). The node size on every graph is proportional to the individuals’
degree and edge widths are proportional to the weighted value of the relation (family ties have
thicker lines). ................................................................................................................................ 113
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