Download Salmonella Enteritidis in backyard poultry flocks in Alberta: are

Salmonella Enteritidis in backyard
poultry flocks in Alberta
Are owners at risk?
ILONA HOUSTON
ADED ROUNDS
MARCH 20, 2017
1
OneHealth
Interconnectedness of human and animal (and
environmental) health demands an
interdisciplinary approach
Zoonoses and foodborne diseases
33 million DALYs attributable to foodborne
diseases (WHO, 2015)
http://www.phgfoundation.org/file/16911/
2
Salmonella
Salmonella spp.
● Gram negative rods; two species and many many
many serovars with varying host-specificities
● Numerous diseases in poultry
● Numerous diseases in humans
>93 million cases of gastroenteritis and >100,000 deaths due to
Salmonella infection globally/year
Serovar of interest: Salmonella enterica Enteritidis (SE)
second most common serotype isolated in human
salmonellosis cases
http://www.sc.chula.ac.th/agtechinter/
3
Epidemiology and pathology of SE
 Poultry
● often introduced to a flock via infected eggs/chicks
●horizontal transmission: contaminated feces, litter, fomites
● wildlife, rodents, insects
●vertical transmission: eggs
●adult birds often asymptomatic carriers: shed bacteria
 Humans
● direct contact with infected animals
● indirect contact/environmental transmission
● foodborne (eggs, poultry)
●acute onset typically self-limiting diarrhea, non-specific flu-like illness
●children, elderly and immunocompromised most vulnerable
●severe cases may require hospitalization, bacteremia can lead to mortality
http://greenbeandelivery.com/healthytimes/news/going-local-for-breakfast/
4
Control of SE and small flocks
● Largely successful integrated SE control programs for commercial flocks in
Europe and North America feature sampling and routine testing for SE,
including hatcheries
●SE is reportable in poultry: positive results require
quarantine/depopulation/C&D and enhanced sampling protocol to ensure
premises decontaminated
●Eggs from commercial facilities that test SE+ may be held from distribution
or pasteurized for safety
●Backyard flocks: Growing in popularity, poorly characterized
demographics, no central representative organization, challenges in applying
similar control measures, enforcing regulations and distributing information
●Non-commercial production is also often thought of as a higher risk due to
lower biosecurity measures and closer interaction between birds
http://agr.georgia.gov/backyard-poultry-owners.aspx
5
Outbreak timeline
OFFICIAL
START OF
OUTBREAK
START OF
HIGH RISK
HATCHING
PERIOD ONSET OF
HUMAN
CASES
1 Mar
PHAC POSTS
PUBLIC HEALTH
ALERT
AH ACTIVATES
INVESTIGATION
1 Apr
FIRST REPORTED
HUMAN CASE:
UNCONFIRMED
LAST
NEGATIVE SE
RESULT FOR
HATCHERY
1 May
POSITIVE SE
RESULT FOR
HATCHERY
LAST POSITIVE SE AT
HATCHERY END OF
HIGH RISK HATCHING
PERIOD
1 Jun
END OF
HUMAN
CASES
REPORTED
1 Jul
6
Aims and Objectives
● describe and analyze data gathered by MoAF during the
investigation SE outbreak in backyard flocks in Alberta
● interpret these in conjunction with the findings revealed by the
parallel public health authority investigation
 to assess the risk of salmonellosis posed to backyard flock owners
by birds from a known-contaminated source and those confirmed to
be infected with SE, and further identify opportunities and
recommendations for mitigation of the threat of SE to public health.
Sick
humans
7
Methods
● Data collection by MoAF:
 Gathered during outbreak investigation - similar to an observational cross-sectional study, using a
convenience sample of self-selected owners who purchased chicks from the identified hatchery source during
the defined risk period, received notification of the outbreak and elected to contact the OCPV
● Environmental sampling kits  internally validated industry-accepted RT-PCR method
●PHAC: further molecular diagnostics (serotyping, phage typing, PFGE, MLVA, and WGS)
Outcome of interest: self-reported illness at the household level (Y/N)
Exposures of interest: SE sample kit result (+/-), morbidity/mortality in flock (Y/N), layers on premises (Y/N)
● Preliminary analysis for association was performed using Pearson’s chi squared test at p<0.05 significance level
● More robust multivariable analysis of association, logistic regression was used to test the binary variables with
the outcome of any reported illness in humans per household.
8
9
Results
Variable
Positive
(n)
Proportion
Negative
(n)
Proportion
(%)
Total (n)
Self-reported illness at the
household level
53
19.85%
214
80.15%
267
SE environmental sample
result
159
44.92%
[39.65,50.26]
195
55.08%
[49.74, 60.35]
354
Bird morbidity/mortality
63
23.86%
201
76.14%
264
Layers on premises
136
92.52%
11
7.48%
147
10
Results
Variable
Pearson’s chi2
p-value
Flock tested SE+
20.6473
<0.001*
Morbidity/mortality reported
in flock
7.4935
0.006*
Layers on premises
2.6325
0.105
Univariate Pearson’s chi2 analysis of the association between predictor variables and outcome of self-reported illness in
humans; degrees of freedom = 1. * Significant at p<0.05
11
Results
Odds Ratio
95% CI
p-value
SE+
Morbidity/mortality reported in flock
Layers on premises
4.49
2.48
0.334
2.27, 8.89
1.27, 4.18
0.08, 1.32
<0.001*
0.007*
0.118
Adjusted
SE+
Morbidity/mortality reported in flock
4.75
1.95
2.28, 9.86
0.97, 3.92
0.0633
50.63
4.72, 543.12
0.001*
Self-reported illness in humans
Layers on premises
SE+
12
Public Health Investigation Findings:
● median time between receiving birds and the onset of symptoms
was 10 days (1-78)
● ~ two thirds of people became ill in the two weeks following
obtaining affected poultry
● majority of case patients (87%) reported direct contact with the
poultry and their environment
 79% handled poultry directly; 10% reported kissing birds
● 82% reported exposure to poultry at home
 poultry were kept inside the home in 17% of cases
● 56% of owners surveyed had knowledge of the link between
salmonellosis and contact with poultry.
● PHAC diagnostics (serotype, PFGE, MLVA, WGS) results revealed
human patients all infected by the same strain, supporting a single
source
The majority (86%) of poultry samples submitted by owners to MoAF
were consistent with these results
https://www.youtube.com/watch?v=mi80y6FP21s
Centre for Foodborne Environmental and Zoonotic Infectious Diseases, Outbreak management Division report.
13
Discussion
Conclusions: statistically significant association between self-reported illness
in humans and backyard poultry flocks that test positive for SE.
Sick birds: did not improve the multivariate logistic model of association,
possibly due to the ability for infected birds to shed the bacteria while
remaining asymptomatic.
 morbidity in birds may also have gone undetected and thus unreported by
owners, particularly inexperienced or new owners who are unfamiliar with
poultry health; this study does not capture symptoms nor mortality rates,
and did not include testing for other pathogens
Role of layers: included as a variable due to transovarial transmission
infection of layers already present in the flock by infected chicks; has
implications for time period before onset of symptoms, and owners whose
flock tests positive and they maintain layers in the flock or inadequately
decontaminate premises before introducing new layer birds.
 Analysis revealed that when layers were reported on farm, there was
approximately a fiftyfold increase odds of that flock having a positive SE test
result. Possible explanations for this may be that laying breeds were sent out
during a period of higher contamination from the hatchery, that most flocks
contained layers, or that there are other unknown and unmeasured
characteristics of flocks that contain layers?
Sick
humans
14
Discussion
● PHAC diagnostics :reliable, robust and specific support for the relatedness of the SE
isolates
● vast majority of flock samples in AB were this same strain supports that prevalence
of SE found in backyard flock samples is due to the outbreak, rather than representative
of high levels of endemic SE that were being picked up incidentally during the
investigation.
Outbreak prevalence: 44.9% (convenience sample, very high)
Australia: 10%
Iran, Uruguay: 3.5-5.8%
Ontario: <1%
7 flocks yielded non-outbreak related Salmonella: Insight into the baseline prevalence?
● 53 owners reported illness in the household to MoAF; PHAC confirmed 35 human cases
 limitations of using self-reported illness? Barriers to diagnosis? FBDs are thought to be
largely underreported and under-diagnosed, these numbers may support this
15
Conclusions Recommendations
●Surveillance:
Establish baseline SE prevalence and characterize the
backyard flock sector (practices)
●Education and awareness to mitigate risks to owners
and the general public
84% of backyard flock owners in a U.S. survey think
that eggs and meat from their own flock is safer than
commercial animal products
Follow-up with owners regarding decontamination,
ongoing management/biosecurity
●Hatchery as a focus for prevention, contact point with
the public and aid in distribution of materials/information
●Consideration of under-reporting and under-diagnosis
of SE
16
https://memegenerator.net/instance/56529202
Limitations
● Generalizability of these findings has some limitations: outbreak scenario, convenience
sample, self-selected participants limited to AB, ~25% of owners presumed to have received
contaminated chicks submitted samples…
 representativeness of this small sample of the entire backyard flock population of Alberta,
or Canada should be carefully considered
● missing values
● convenience sample
● numerous potential sources of bias
● reliability of SE test results
17
So!
There is strong evidence to support the conclusion that during this outbreak scenario, yes.
18
Acknowledgements
I would like to extend sincere gratitude for the support by the Alberta Ministry of Agriculture
and Forestry, in providing funding, access to data, and the expert contributions by the Animal
Health Branch.
In particular, Drs. Keith Lehman, Chunu Mainali, Simon Otto and Delores Peters for their work
towards supporting the process of allowing me to collaborate with AF on this project, and for
providing me with not only the necessary information to complete the work but also invaluable
insight into this investigation.
Additional thanks to Robin King, Senior Laboratory Scientist, for providing me with information
on molecular biology and testing processes, and to Dr. Simon Otto for his assistance with
statistical analyses. I would also like to express my appreciation of the thorough and considerate
input and support provided to me by my LSHTM PHM 305 Project mentor, Dr. James Rudge.
19
Questions?
20
References
Acheson D., Hohmann E.L. Nontyphoidal salmonellosis. 2001. Clinical Infectious Diseases 32:263-269.
Guard-Petter J. The chicken, the egg, and Salmonella enteritidis. 2001. Environmental Microbiology 3:421-430.
Pollock S.L., Stephen C., Skuridina N., Kosatsky T. Raising chickens in city backyards: the public health role. 2012. Journal of Community Health 37:734-742.
Animal Health Act, Reportable and Notifiable Diseases Regulation. Alberta Regulation 129/2014. Accessed December 16, 2015
http://www.qp.alberta.ca/1266.cfm?page=2014_129.cfm&leg_type=Regs&isbncln=9780779781201
Hale C.R., Scallan E., Cronquist A.B., Dunn J., Smith K., Robinson T. Lathrop S., Tobin-D’Angelo M., Clogher P. Estimates of enteric illness attributable to
contact with animals and their environments in the United States. 2012. Clinical Infectious Diseases 54:S472-S478.
Roegner A., Giannitti F., Woods L>W., Mete A., Puschner B. Public health implications of lead poisioning in backyard chickens and cattle: four cases. 2013.
Journal of Veterinary Medicine Research and Reports 4:11-20.
Howard Z.R., O’Bryan C.A., Crandall P.G., Ricke S.C. Salmonella Enteriditis in shell eggs: Current issues and prospects for control. 2012. Food Research
International 45:755-764.
Smith G., Dunipace S. How backyard poultry flocks influence the effort required to curtail avian influenza epidemics in commercial poultry flocks. 2011.
Epidemics 3:71-75.
Lebert, L., Janecko, N., Reid-Smith, R. J., Rubin, J. E., Agunos, A., Deckert, A, Martz, S., Reid, M.A., and McEwen, S.A. Antimicrobial resistance in E. coli and
Salmonella from small holder chickens 4th ASM Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens. May 8-11, 2015.
Washington, DC.
Thomas M.K., Murray R., Flockhart L., Pintar K., Pollari F., Fazil A., Nesbitt A., Marshall B. Estimates of the burden of foodborne illness in Canada for 30
specific pathogens and unspecified agents, circa 2006. 2013. Foodborne Pathogens and Disease 10:639-648.
Liebana E., Garcia-Migura L., Clouting C., Clifton-Hadley F.A., Breslin M., Davies R.H. Molecular fingerprinting evidence of the contribution of wildlife
vectors in the maintenance of Salmonella Enteritidis infection on layer farms. 2003. Journal of Applied Microbiology 94: 1024-1029.
Tobin M.R., Goldshear J.L., Price L.B., Graham J.P., Leibler J.H. A framework to reduce infectious disease risk from urban poultry in the United States. 2015.
Public Health Reports 130:380-391.
Loharikar A. et al. Four multistate outbreaks of human Salmonella infections associated with live poultry contact, United States, 2009. 2012. Zoonoses
Public Health 59:347-354.
USDA. U.S. Department of Agriculture. Poultry 2010. Reference of the health and management of chicken flocks in urban setting sin four U.S. cities, 2010.
USDA Animal and Plant Health Inspection Service-Veterinary Services, Centers for Epidemiology and Animal Health, Fort Collins CO
Majowicz S.E., J. Musto, E. Scallan, F.J., Angulo, M. Kirk, S.J. “Brian, T.F. Jones, A. Fazil, and R.M. Hoekstra. 2010. The Global Burden of Nontyphoidal
Salmonella Gastroenteritis. Clinical Infectious Diseases 50:882-889.
Whitehead M.L., Roberts V. Backyard poultry: legislation, zoonoses and disease prevention. 2014. Journal of Small Animal Practice 55:487-496.
Bavinck V., Bouma A., van Boven M., Bos M.E., Stassen E., Stegeman J.A. The role of backyard poulty flocks in the epidemic of highly pathogenic avian
influenza virus (H7N7) in the Netherlands in 2003. 2009. Preventive Veterinary Medicine 88:247-254.
Beam A., Garber, L., Sakugawa J., Kopral C. Salmonella awareness and related management practices in U.S. urban backyard chicken flocks. 2013.
Preventive Veterinary Medicine 110:481-488
Behravesh C.B., Brinson D., Hopkins B.A., Gomez T.M. Backyard Poultry Flocks and Salmonellosis: A recurring, yet preventable public health challenge.
2014. Food Safety 58:1432-1438.
Belanger P., Tanguay F., Hamel M., Phypsers M. CCDR: Canadian Communicable Disease Report Volume 41-11, 2015. Foodborne Illness. An overview of
foodborne outbreaks in Canada reported through Outbreak Summaries: 2008-2014.
Bland, M. Salmonella prevention measures for small backyard flock owners. 2015. Journal of Exotic Pet Medicine 24:141-155.
Butler A.J., Thomas M.K., Pintar K.D.M. Expert elicitations as a means to attribute 28 enteric pathogens to foodborne, waterborne, animal contact and
person-to-person transmission routes in Canada. 2015. Foodborne Pathogens and Disease 12:335-344.
Wilkins M.J., Bidol S.A., Boulton M.L., Strobierski M.G., Massey J.P., Robinson-Dunn B. Human salmonellosis associated with young poultry from a
contaminated hatchery in Michigan and resulting public health interventions, 1999 and 2000. 2002. Epidemiology and Infection129:19-27.
Majowicz S.E., V.L. Edge, A. Fazil, B.W. McNad, K.A. Dore, P. N.Sockett, J.A. Flint, D. Middleton, S.A. McEwen, and J.B. Wilson. 2005. Estimating the underreporting rate of Infectious gastrointestinal illness in Ontario. Canadian Journal Public Health 96:178-181.
CDC Centre for Disease Control. 2016. Eight multistate outbreaks of human Salmonella infections linked to live poultry in backyard flocks. Accessed 08-192016. Available from: https://www.cdc.gov/salmonella/live-poultry-05-16/index.html
Manning J., Gole V., Chousalkar K. Screening for Salmonella in backyard chickens.2015. Preventive Veterinary Medicine 120:241-245.
CDC Centre for Disease Control: Risk of human Salmonella infection from live baby poultry Accessed 12/10/2015. Available from
http://cdc.gov.features/salmonellababybirds/.
CDC Centre for Disease Control: OneHealth. Accessed 11/11/2015, Available from: http://www.cdc.gov/onehealth/
CFEZID/OMD. Centre for Foodborne Environmental and Zoonotic Infectious Diseases, Outbreak Management Division. Internal Document: Multiprovincial/territorital outbreak of Salmonella Entertidis (SE) associated with mail-order chicks in Alberta, British Columbia, Saskatchewan, Northwest
Terriroties and Manitoba [2015-681].
WHO. World Health Organization estimates of the global burden of foodborne diseases. Foodborne diseases burden epidemiology reference group 20072015. 2015.
Accessed 07/07/2016 Available from: http://www.who.int/foodsafety/publications/foodborne_disease/fergreport/en/
Marine J.C., Jones B.A., Hendricks S., Masry E., Jobre Y., Jost C.C. Experiences in participatory surveillance and community-based reporting systems for
H5N1 highly pathogenic avian influenza: A case study approach. 2014. EcoHealth 11:22-35.
Mete A., Giannitti B., Barr B., Woods L., Anderson M. Case Report- Causes of mortality in backyard chickens in Northern California: 2007-2011. 2013. Avian
Diseases 57:311-315.
Oscar T.P. A quantitative risk assessment model for Salmonella and whole chickens. 2004. International Journal of Food Microbiology 93:231-247.
Conan A., F.L. Goutard, S. Sorn and S. Vong. Biosecurity measures for backyard poultry in developing countries; a systematic review. 2012. BioMedCentral
Veterinary Research 8:240.
Denagamage T., Jayarao B., Patterson P., Wallnder-Pendleton E., Kariyawasam S. Risk Factors associated with Salmonella in laying hen farms: systematic
review of observational studies. 2015. Avian Diseases 59:291-302.
EFSA. European Food Safety Authority. Salmonella. Accessed 11/11/2015. Available from: http://www.efsa.europa.eu/en/topics/topic/salmonella
Elkhoraibi C., Blatchford R.A., Pitesky M.E., Mench J.A. Backyard chickens in the United States: a survey of flock owners. 2014. Poultry Science 98:29202931.
OIE. Terrestrial Animal Health Code Chapter 6.5. Prevention, detection and control of Salmonella in poultry. PHAC. Public Health Agency of Canada. Public
Health notice- Outbreak of Salmonella infections related to contact with live baby poultry. July 23, 2015.
Accessed: 12/11/2015 Available from: http://www.phac-aspc.gc.ca/phn-asn/2015/salmonella-eng.php
PHAC. Public Health Agency of Canada.
PulseNet Canada Overview. Accessed September 3, 2015. https://www.nml-lnm.gc.ca/Pulsenet/overview-apercu-eng.htm
Public Health Notice- Outbreak of Salmonella infections related to contact with live baby poultry. Accessed December 11, 2015. http://www.phacaspc.gc.ca/phn-asp/2015/salmonella-eng.php
Pires S.M., Vieira A.R., Hald T., Cole D. Source Attribution of human salmonellosis: An overview of methods and estimates. 2014. Foodborne Pathogens
and Disease 11:667-676.
Gaffga N.H., Behravesh B.C., Ettestad P.J., Smelser C.B., Rhorer AR., Cronquist A.B., Cornstock N.A., Bidol S.A., Patel N.J., Gerner-Smidt P., Keene W.E.,
Gomez T.M., Hopkins B.A., Sotir M.J., Angulo F.J. Outbreak of salmonellosis linked to live poultry from a mail-order hatchery. 2012. New England Journal
of Medicine 366:2065-2073.
Pires S.M. Assessing the applicability of currently available methods for attributing foodborne disease to sources, including food and food commodities.
2013. Foodborne Pathogens and Disease 10:206-213.
Grunkemeyer V.L. Zoonoses, public health and the backyard poultry flock. 2011. Veterinary Clinical Exotic Animals 14:477-490.
Pires S.M., Vigre H., Makela P., Hald T. Using outbreak data for source attribution of human salmonellosis and campylobacteriosis in Europe. 2010.
Foodborne Pathogens and Disease 7:351-361.
21