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Epidemiologic Study

of Highly Pathogenic

Avian Influenza H5N2

among Turkey Farms,

2015

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Minnesota poultry farms affected with highly pathogenic H5N2 avian influenza�

Source: USDA-APHIS-Veterinary Services

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An outbreak of highly pathogenic H5N2 avian influenza (HPAI) occurred among turkey

farms between early March and early June 2015. The Minnesota Board of Animal Health reported that 104 operations in

23 counties in Minnesota were affected by the virus. The economic damage to Minnesota alone has been estimated at

more than $647.2 million, including $171.7 million in lost wages, salaries, and benefits, and 2,500 jobs were affected,

according to a University of Minnesota Extension study.

Since then, no new cases have appeared, but scientists and poultry producers remain concerned that another outbreak

could occur. An initial investigation by the U.S. Department of Agriculture’s Animal Plant and Health Inspection Service

(USDA–APHIS) described the location, time of outbreak, and management practices employed for each affected farm.

To support ongoing efforts to identify farm-level risk factors, the University of Minnesota College of Veterinary Medicine’s

Center for Animal Health and Food Safety (CAHFS), with funding and cooperation from a large integrated turkey company

and input from several state and federal agencies, conducted a case-control study to identify potential risk factors

associated with this past spring’s HPAI outbreak. This investigation was limited to turkey flocks in the Upper Midwest.

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THE STUDYTo identify possible risk factors, the research team

developed a detailed survey that asked turkey farmers

questions about the farm and surrounding environment,

presence of wild birds, and farm management practices.

The survey was focused on the two-week period prior to

HPAI diagnosis for case farms and a similar assigned

two-week period for control farms. A total of 83 (43 case

and 40 control) farmers were interviewed. Statistical

analysis was used to compare the occurrence of risk or

protective factors between case and control farms. The

final risk model included farms that were located in

affected regions and included 63 turkey farms in the

Upper Midwest: 37 case farms with known outbreaks and

26 control farms.

In addition to comparing factors between all 63 case

and control farms, the research team also investigated

whether there were differences in risk or protective

factors over the course of the outbreak. As last spring’s

HPAI outbreak persisted from early March to early June,

peaking around April 22, the team compared case and

control farms with reference periods before April 22

(early in the outbreak) and those after April 22 (late

in the outbreak). The early period corresponded to wild

bird migration, a potential risk factor.

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FINDINGSIn terms of farm characteristics, case and control farms were similar in size, number of employees, and type of operation.

Overall, study findings suggest that the outbreak was initiated through multiple introductions either from wild birds and/

or a contaminated environmental reservoir. It is likely that the outbreak was then perpetuated by several factors including

biosecurity breaches and the intensity of the outbreak in areas where farms are in close proximity to each other. Despite

existing biosecurity measures, the outbreak persisted over several months.

One important and significant risk factor in this recent H5N2 HPAI outbreak was proximity to other turkey operations/

poultry farms and to confirmed HPAI infected farms. Case farms, on average, were closer to confirmed HPAI farms than

were control farms (1.5 miles versus 5.2 miles).

Previous studies have shown that influenza viruses can survive cold temperatures in soil environments. Potential

contamination of these fields with droppings from migrating birds could serve as a source of infection. This study found

that actively working (tilling or discing) fields closest to turkey barns within the 14-day reference period was a risk factor.

This was potentially due to soil disruption and the creation of airborne particles that could carry the virus. When stratified

by time period, this risk factor was only observed early in the outbreak, suggesting it played a role in introduction but not

lateral spread.

Description Control Farms Case Farms P value

Number of birds on farm median 51,847 56,930 0.91Number of employees median 2.5 2 0.63

Stage(s) of production present on farm

Brooder 11 (42.3%) 11 (29.7%) 0.30Grower 24 (92.3%) 35 (94.6%) 1.00 Breeder 1 (3.9%) 1 (2.7%) 1.00

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This study also found the use of rendering to dispose of dead birds to be

a risk factor. This association has been observed in other previous HPAI

poultry outbreaks as well. Ideally, rendering trucks should be thoroughly

disinfected before moving between farms, and rendering bins should

be placed away from the production barns.

Previous outbreaks have also shown that biosecurity practices are

important drivers for outbreaks. In this investigation, good and

uniform biosecurity protocols for farm workers had a protective effect,

particularly in the early period of the outbreak. Specifically, control

farms tended to institute more biosecurity protocols for personnel compared to case farms.

As shown in the table below, some factors also found to be associated with HPAI diagnosis were less clear in interpretation,

including observing wild birds near barns or wild mammals near bird disposal areas and high visitor biosecurity protocols

in place. Late in the outbreak, non-asphalt roads and vehicle wash stations appear to be risk factors. As these risk

factors are unique to the late-outbreak period, they could indicate an overall high level of environmental contamination.

The results do indicate an opportunity to re-evaluate standard operating procedures for vehicle disinfection.

RISK FACTORS IDENTIFIED IN THE STUDY

Full-outbreak risk factors for HPAI Odds ratio (95% CI)Close proximity to other farms 46.14 (5.96 - 357.55)

Render dead birds 9.80 (1.46 - 65.96)

Tilled in last 14 days 6.46 (1.36 - 30.78)

Wild mammals near barns 0.14 (0.02 - 1.06)

Early-outbreak risk factors for HPAI Odds ratio (95% CI)Tilled in last 14 days 13.88 (1.04 - 184.85)

High visitor biosecurity 7.92 (0.88 - 71.41)

High worker biosecurity 0.07 (0.01 - 0.96)

Late-outbreak risk factors for HPAI Odds ratio (95% CI)Use of vehicle wash station/spray area 12.40 (0.94 - 163.52)

Non-asphalt roads 10.05 (0.65 - 156.49)

Wild birds near dead bird disposal 0.12 (0.02 - 0.72)

Note: Odds ratio means farms with the factor have X times greater or less odds of having

an outbreak than farms without that particular factor. The 95% confidence intervals indicate

that 95% of the time the true effect estimate is expected to be within this range.

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THE TAKE-AWAYUnderstanding disease transmission risk factors is critical to developing strategies to reduce the spread and severity

of future HPAI exposures and outbreaks. Results from this study suggest the spring 2015 outbreak was associated

with multiple environmental and biosecurity factors. Moreover, risk factors differed between early- and late-outbreak

infections. It is unclear whether these differences were related to changes in exposure over time or changes in biosecurity

measures during the course of the outbreak.

It is important to note that each turkey operation is different with different barn types, topography, and practices. General

recommendations need to be tailored for each individual farm. Based on these initial findings, some general precautions

as a way to reduce HPAI risk exposure may include the following:

• Continue implementation of strict biosecurity management practices.

Good farm worker biosecurity is crucial.

– Place rendering bins away from production barns and require that

rendering trucks be disinfected before entering and leaving the farm.

– Develop vehicle wash station biosecurity best practices.

• Consider planting perennial crops, such as alfalfa, in fields closest

to turkey farms that do not involve early spring tilling of fields.

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STUDY LIMITATIONSThis study reflects a small subset of infected and non-infected farms associated with a large integrated turkey operation,

and may not reflect other operations. Also, this study reflects a specified region of the country—results should be viewed as

hypothesis-generating rather than confirmatory. Additional experimental studies are needed to improve some biosecurity

protocols (i.e., best practices for vehicle wash stations).

STUDY COLLABORATORS AND PARTICIPANTSUniversity of Minnesota Center for Animal Health and Food Safety

Jennie-O Turkey Store

USDA-Animal and Plant Health Inspection Service

Minnesota Board of Animal Health

Minnesota Department of Health

Minnesota Turkey Growers Association

Other turkey experts

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136 Andrew Boss Laboratory • 1354 Eckles Avenue • St. Paul, MN 55108CAHFS@umn.edu • 612-625-8709 • Fax: 612-624-4906