Evaluation of Maryland Backyard Flocks and Biosecurity Practices Author(s): Jennifer M. Madsen, Nickolas G. Zimmermann, Jennifer Timmons, and Nathaniel L. Tablante Source: Avian Diseases, 57(2):233-237. 2013. Published By: American Association of Avian Pathologists DOI: http://dx.doi.org/10.1637/10428-101912-Reg.1 URL: http://www.bioone.org/doi/full/10.1637/10428-101912-Reg.1
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AVIAN DISEASES 57:233–237, 2013
Evaluation of Maryland Backyard Flocks and Biosecurity Practices Jennifer M. Madsen,A Nickolas G. Zimmermann,B Jennifer Timmons,C and Nathaniel L. TablanteAD A
Virginia-Maryland Regional College of Veterinary Medicine, University of Maryland, College Park, MD 20742 B Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742 C Department of Agriculture, Food and Resource Sciences, University of Maryland Eastern Shore, Princess Anne, MD 21853 Received 21 October 2012; Accepted 7 February 2013; Published ahead of print 11 February 2013 SUMMARY. Domesticated poultry are susceptible to infectious and zoonotic diseases and can serve as a transmission source to other bird and human populations. In recent years, the number of noncommercial poultry has been on the rise in the United States. To evaluate potential risks of this growing population, a descriptive epidemiologic survey was conducted among Maryland backyard flocks. Owner and flock demographics were characterized as well as management practices such as husbandry, human-tobird interaction, bird exposure risks, poultry health status, and biosecurity. Data from the 41 returned questionnaires indicated a median flock size of 38 birds (range, 3–901). Chickens accounted for 86.5% of the reported birds overall. Just over half of the owners (51.2%) kept chickens only, with the remaining backyard flocks consisting of chickens, other gallinaceous species, waterfowl, or a combination. Of flocks with multiple species, 70.0% of owners did not keep them separate. Almost two thirds of owners (61.0%) had kept poultry for #5 yr, with 44.0% of all flocks on free range. Over the past 2 yr, predation was the highest cause of specific mortality (57.1%) followed by disease (30.2%), unknown (8.7%), and injury (4.0%), and over half of owners (56.1%) reported signs of disease in their flock within the last 6 mo. Biosecurity practices were highly variable among flocks. Data from this study identified gaps in the disease prevention and biosecurity practices of backyard flocks. These results can be useful in developing educational extension and outreach programs as well as policies, in efforts to further mitigate the spread of diseases. RESUMEN. Evaluacio´n de las parvadas de traspatio en el estado de Maryland y de sus pra´cticas de bioseguridad. Las aves dome´sticas son susceptibles a las enfermedades infecciosas y zoono´ticas y pueden servir como una fuente de transmisio´n a otras aves y a poblaciones humanas. En an˜os recientes, el taman˜o de la avicultura no comercial ha ido en aumento en los Estados Unidos. Para evaluar los riesgos potenciales de esta poblacio´n en crecimiento, se llevo´ a cabo un estudio epidemiolo´gico descriptivo en parvadas de traspatio de Maryland. La demografı´a de las parvadas y de los propietarios fue caracterizada ası´ como las pra´cticas de manejo, tales como el manejo de crianza, la interaccio´n entre aves y humanos, los riesgos de exposicio´n de las aves, el estado de salud de las aves y su bioseguridad. Los datos de los 41 cuestionarios indicaron un taman˜o de parvada promedio de 38 aves (rango, de tres a 901 aves). Los pollos representaron el 86.5% de las aves reportadas en general. Un poco ma´s de la mitad de los propietarios (51.2%) mantuvo pollos solamente, mientras que las parvadas restantes consistieron de pollos, de otras especies de gallina´ceas, aves acua´ticas, y sus combinaciones. De las parvadas con mu´ltiples especies, el 70.0% de los propietarios no mantuvieron las diferentes especies alojadas por separado. Casi dos tercios de los propietarios (61.0%) habı´an mantenido aves de corral por ma´s de cinco an˜os, con un 44.0% de las parvadas mantenidas en pastoreo. En los dos u´ltimos an˜os, la depredacio´n fue la mayor causa de mortalidad especı´fica (57.1%) seguida por enfermedades (30.2%), por causas no determinadas (8.7%) y por lesiones (4.0%), y ma´s de la mitad de los propietarios (56.1%) informaron la presencia de signos de enfermedad en sus parvadas en los u´ltimos seis meses. Las pra´cticas de bioseguridad fueron muy variables entre las parvadas. Los datos de este estudio identificaron deficiencias en la prevencio´n de enfermedades y en las pra´cticas de bioseguridad en las parvadas de traspatio. Estos resultados pueden ser u´tiles para el desarrollo de programas educativos y de extensio´n, ası´ como para las polı´ticas y esfuerzos para disminuir la diseminacio´n de las enfermedades. Key words: backyard flock, biosecurity, epidemiology, zoonotic disease, poultry, risk factors, avian influenza, education Abbreviations: AI 5 avian influenza; HPAI 5 highly pathogenic avian influenza; ILT 5 infectious laryngotracheitis; LPAI 5 low pathogenic avian influenza; MDA 5 Maryland Department of Agriculture; MG 5 Mycoplasma gallisepticum; NAHMS 5 National Animal Health Monitoring System; USDA 5 U.S. Department of Agriculture
Backyard flock ownership is growing in popularity across the United States from country farms to urban residences, and as the numbers of unregulated poultry increase, so does the need for disease surveillance and biosecurity education (19). Domesticated poultry are susceptible to infectious and zoonotic diseases and can serve as transmission sources to other bird and human populations (6,10,13). In recent years, some states, including Maryland, have begun taking an active approach to surveillance by requiring flock registration and testing before participating in fair or auction markets, operating hatcheries, or selling local eggs or poultry (8). However, this population only accounts for a small percentage of owners based on the U.S. Department of Agriculture (USDA), National Animal Health Monitoring System (NAHMS) 2004 survey that reported that only 11.2% of owners ranked these D
Corresponding author. E-mail: [email protected]
categories (extra income and clubs/social interactions) as high and very high as primary reasons for keeping poultry (18). Poultry can carry a variety of infectious diseases of economic importance, and they are capable of subclinically harboring human pathogens. This capability warrants consideration in backyard flocks because biosecurity practices are generally not monitored or enforced. Salmonella poisoning in recent years has been linked to contact with contaminated poultry. From 2004 to 2011, 316 cases of Salmonella Montevideo from 43 states were reported to be the result of handling infected chicks, ducklings, and live poultry (6). Avian influenza (AI) virus is another major pathogen of concern that can cause mild-to-severe respiratory disease in gallinaceous species. It also is capable of causing disease in humans, although rare. Low pathogenic AI (LPAI) and highly pathogenic AI (HPAI) viruses have been responsible for the culling of millions of birds worldwide, costing billions in containment and production losses. In 2004, an
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Table 1. Backyard flock species distribution and median flock size among the surveyed regions of Maryland. Northern Maryland
No. of flocks Median flock size SpeciesB Chickens Turkeys Ducks Guinea fowl Pheasants Geese Peacocks Chuckers Doves Total
Southern Maryland
Eastern Shore
Overall (%)
20 40
12 32
9 42
41 38
2174 216 38 50 0 13 4 0 3 2498
328 8 107 33 33 2 6 3 0 520
1173 35 12 0 0 9 0 0 0 1229
3675 259 157 83 33 24 10 3 3 4247
RangeA
3–901
(86.5) (6.1) (3.7) (2.0) (0.8) (0.6) (0.2) (0.07) (0.07)
3–901 0–210 0–65 0–25 0–30 0–8 0–6 0–3 0–3
A B
Number of birds per flock. Total number of birds by species.
LPAI H7N2 outbreak hit Maryland and Delaware and resulted in the costly depopulation of 378,000 and 84,000 chickens, respectively (2,14). Although no human cases of AI were reported, transmission of influenza A viruses from poultry to people has been documented previously in North America (3,4). These cases were treatable and made a full recovery; however, in other parts of the world, the HPAI H5N1 strain has caused 607 human cases and 358 deaths, resulting in an extremely high case fatality rate (10,13,21). Transmission of AI viruses through trade of infected poultry and contaminated equipment is considered one of the main means of spread, but with the use of biosecurity, the risk of introducing disease can be prevented or reduced (11,12,13). In an effort to control the transmission of poultry diseases, some U.S. states require all poultry owners to register flocks with their state’s department of agriculture. In 2005, the Maryland General Assembly passed legislation mandating backyard poultry registration. As of June 2011, there have been 3258 backyard flocks registered with the Maryland Department of Agriculture (MDA) (9). Understanding backyard flock management practices has economic importance as well. Five counties in Maryland lead the nation in broiler production. According to 2010 Delmarva Poultry Industry, Inc. data, Somerset County ranked 25th, Worcester County 26th, Wicomico County 36th, Caroline County 40th, and Dorchester County 63rd among all U.S. counties (5). This study aimed to characterize Maryland backyard poultry and to identify gaps in biosecurity practices in an effort to develop better education programs and healthier flocks. MATERIALS AND METHODS Study design. Survey locations were divided into three regions of Maryland by counties: Northern (Frederick and Carroll), Southern (St. Mary’s and Charles), and Eastern Shore (Caroline, Dorchester, Talbot, Wicomico, and Worcester). County selection was based on the high proportion of registered backyard flock owners as well as relative location to commercial industries and auction markets. In May 2011, the MDA confidentially mailed 1000 informational letters and return postcards to poultry owners enrolled in the Maryland Poultry Registration Program. Backyard flocks were defined using the NAHMS Poultry 2004 guidelines as residences with fewer than 1000 birds (other than pet birds or in addition to pet birds). If poultry owners wished to participate, they were asked to contact the University of Maryland via email or via prepaid return postcards.
Participants were eligible for the study if they lived within Maryland, owned domesticated fowl, and had a flock size fewer than 1000 birds. Respondents were offered a free diagnostic health status report of their flock as an incentive to participate in the study. Upon agreement to participate, owners were sent an information sheet, questionnaire, and consent form providing further details of the study, including the risks and benefits of participation. This study was approved in accordance with the University of Maryland’s Institutional Review Board (110335) and Federal Policy for the Protection of Human Subjects (45 CFR 46). Questionnaire. A four-page questionnaire, adapted from USDA Poultry 2010 and previous publication by Tablante et al. was created to determine biosecurity factors that may be associated with the health status of small flocks (17,18,19). Upon state and academic review by the Maryland state veterinarian, assistant state veterinarians, one animal health inspector from the MDA, and poultry extension agents with the University of Maryland, a questionnaire and information sheet were mailed to backyard flock owners who agreed to participate. Participants were asked to self-report information on the number and species of poultry reared, presence of other animals, animal husbandry, opportunities for interaction between wild birds and poultry, flock biosecurity measures, and health status of poultry. The questionnaire is available upon request.
RESULTS
Backyard flock demographics. Of the 1000 contacted backyard flock owners, 41 (4.1%) agreed to participate and all completed surveys. From the returned surveys, we determined that flock sizes ranged from three to 901 birds, with the median of 38 birds per flock. All owners reported having chickens on their property, with just over half (51.2%) having chickens as the only species of domestic poultry. Chickens accounted for 86.5% of the reported birds overall (Table 1). The remaining flocks had a mix of chickens and other domestic bird species, with 17.1% keeping chickens and turkeys; 24.4% raising chickens and waterfowl; 9.8% keeping chickens, turkeys, and waterfowl; and 14.6% having chickens, waterfowl, and game fowl species on the property. Only two flocks had peafowl (Pavo spp.), with one peafowl flock also having chickens, turkeys, waterfowl, and game fowl. The number of species in a flock ranged from one to six, with the median count of one. Sixty-one percent of surveyed owners have kept backyard poultry for #5 yr, whereas 24.4% have had poultry between 6 and 10 yr and 14.6% have kept poultry for .10 yr. The predominant reason for keeping poultry was personal consumption of eggs (56.1%),
Biosecurity in Maryland backyard flocks
Table 2. Percentage of backyard flock characteristics as reported by flock owners. Characteristic
%
Flocks with multiple species Chickens and turkeys Chickens and waterfowlA PoultryB and waterfowlA PoultryB and peafowl (peacock) PoultryB and game fowlC Chickens, waterfowl,A and game fowlC
17.1 24.4 9.8 2.4 7.3 14.6
Duration of ownership #12 months 13 mo–5 yr 6–10 yr .10 yr
17.1 43.9 24.4 14.6
Reason for keeping birds Home egg consumption Selling eggs Selling live birds Pets Home meat consumption Selling meat
56.1 29.3 4.9 4.9 2.4 2.4
Causes of mortality (previous 2 yr) Predation Disease Unknown Injury
57.1 30.2 8.7 4.0
Signs of disease (previous 6 mo) Diarrhea Poor egg production (decrease in or soft or misshapen eggs) Respiratory (coughing, sneezing, nasal secretions, or swollen sinuses) Weight loss or anorexia Neurologic (lack of coordination or weakness) Swelling (head, comb, wattles, or hocks) A
29.2 29.2 9.7 7.3 4.9 0.0
Waterfowl is defined as having ducks or geese. Poultry is defined as having both chickens and turkeys. C Game fowl is defined as having pheasant, guinea fowl, chucker, or doves. B
Fig. 1.
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followed by selling eggs (29.3%). Other owners kept poultry for live sale (4.9%), as pets (4.9%), for home consumption (2.4%), or to sell as meat (2.4%; Table 2). Flock management and exposures. Housing types for poultry was recorded as 39.0% cooped, fenced-in and covered; 17.0% cooped, fenced-in but not covered; 29.3% free range; and 14.7% free range near a water source such as ponds or streams. Of the 20 backyard flocks with multiple species, only six owners (30.0%) keep them separate. Owner and poultry exposure to other animals was variable. Overall, 53.7% of poultry were reported as accessible to wild birds whereas only 9.8% were reported as accessible to waterfowl (Fig. 1). Personal interaction with livestock, such as pigs, sheep, and cattle, was reported by 41.5% of owners, whereas 31.7% of the poultry populations were exposed to livestock. Only five of 41 (12.2%) flocks reported being within a quarter mile of a commercial flock, whereas 68.0% of owners reported being within a quarter mile of other backyard flocks. In the average year, 10 owners visited commercial poultry sites one to 12 times (median 5 7), with three owners coming into contact with commercial birds. In the average year, 10 owners also visited other backyard flocks one to 78 times (median 5 7.5), with nine owners coming into direct contact with birds. Nine owners did not allow visitors, and of those who permitted guests, 73.0% allowed direct contact with birds. Only 4.9% of owners sold birds at a market and 7.3% bought birds from markets. Within the last year, 83.0% of owners purchased new birds. Of those who purchased birds, 17.6% did not isolate them before introduction into the flock. Those who did isolate, on average, separated their new birds for 9–10 wk, with three owners keeping new birds separate indefinitely. Flocks originated from multiple sources, with some individual flock owners obtaining birds from several locations. Mail-order hatcheries were the predominant means of acquiring birds, with 30 owners using online-based hatcheries from other states. Nine owners used local retail feed and farm supply stores, whereas three flock owners purchased birds from commercial poultry houses and another three owners from a private source, such as a friend or from other backyard flocks. Four flock owners purchased birds from county fairs, flea markets, or bird auctions. Flock health. Only one of 41 owners vaccinated birds once they were on the premises. The owner vaccinated for Mycoplasma gallisepticum (MG), infectious laryngotracheitis (ILT) virus, and fowlpox. In the previous 2 yr, owners reported predation as having the highest cause-specific mortality rate (57.1%), followed by disease (30.2%), unknown (8.7%), and injury (4.0%; Table 2). Just over
Percentage of backyard flocks and owners with reported exposure to other animals.
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Table 3. Frequency (percentage) of biosecurity practices reported by backyard flock owners when interacting with flock. Biosecurity factor
Always
Sometimes
Never
Hand washing Designated clothes Dedicated footbath Dedicated footwear Visitor wash hands Visitor designated clothes
65.8 7.3 7.3 31.7 62.5 12.5
22.0 29.3 — — 15.6 3.1
12.2 63.4 92.7 68.3 21.9 84.4
half (56.1%) of owners also reported observing signs of disease in their flock within the past 6 mo. Almost one third (29.2%) of all owners recalled seeing birds with diarrhea, whereas another 29.2% reported a decrease in egg production or soft or misshapen eggs. A few reported respiratory disease symptoms (9.7%), such as coughing, sneezing, nasal secretions, or swollen sinuses, and 7.3% observed weight loss or decreased appetite in their flock. Two owners reported neurologic signs (4.9%) such as lack of coordination or weakness. No owners had birds with swelling of the head, comb, wattles, or hocks. Six backyard flock owners (14.6%) reported that they have previously sent an ill bird to a diagnostic laboratory. Biosecurity practices. For sanitation and decontamination, only three of the owners (7.3%) routinely use a footbath at the entrance to their poultry premises, and two of these three owners also use dedicated footwear. Of the remaining owners, 11 wear a different pair of shoes when entering their poultry area. Although the majority of owners (65.8%) always wash their hands before and after handling their birds, many (63.4%) never wear dedicated clothing (Table 3). More than two thirds of owners clean and disinfect housing and equipment (68.3%), and all but one owner disposes of litter by means of composting (47.4%), setting in a manure pile (31.6%), spreading on fields (18.4%), or having it hauled away (2.6%). Dead birds were usually buried on site (43.6%), composted (20.5%), thrown in trash (15.4%), hauled away (10.3%), or fed to other animals (10.2%). Pest control such as mouse traps or insecticides were used in 39.0% of backyard flock premises. DISCUSSION
Backyard flocks play a role in the ecology and transmission pathways of diseases. However, information on this population remains limited and often presents with unique challenges due to lack of registration databases or flock owner reporting. This study aimed to describe Maryland backyard flocks and to evaluate current management practices. Despite the poor response rate, the results of this study are important as only a handful of other studies have assessed U.S. backyard flock communities with which this study finds both similarities and differences. Several factors may contribute to observed differences between studies, including sample size, climate, population density, culture, state and county regulations, and biosecurity education. A recent cross-sectional study characterizing Colorado backyard flocks also found chickens as the predominant species that were primarily kept for personal consumption (meat and eggs). The Colorado survey found 34.1% of flocks to be free range, whereas 44.0% of surveyed Maryland flocks were reported free range. Among surveyed Maryland flocks, 82.4% reported isolating new birds before introduction into the flock, whereas only 59.9% of sampled Colorado flock owners quarantined new birds (15). However, a Minnesota study found that 82.9% of backyard flock owners separated new birds as well (22).
Unlike the previous reports, this study evaluated the length of ownership to estimate the rate of new flock owners in Maryland; the findings implied that ownership of backyard poultry is on the rise. With the increase in numbers of new flock owners, greater efforts for education on disease prevention are necessary. Almost half of flock owners visited other backyard flocks or commercial poultry sites and several allowed visitors onto their poultry premises. This increase in flock traffic potentially increases the risk of introducing disease via fomites as visitors’ vehicles, boots, and clothing may carry pathogens. Several outbreak investigations have linked fomites in connection with disease spread, such as the 1983 HPAI outbreak in commercial poultry that was associated with human and equipment traffic from New York live bird markets (1). Another study found an association between farms of the 1999 MG outbreak in North Carolina as a poultry grower returned to his flock after visiting an MG-positive farm without changing his contaminated clothing or footwear (20). Although the other half of backyard flock owners did not visit other poultry premises, the proximity of backyard flocks to each other and commercial poultry houses could potentially increase the chances of disease spread. One study designed a model to predict the potential wind-borne transmission of HPAI virus particles between farms given the conditions of the 2003 HPAI outbreak in the Netherlands. The study estimated that 24.0% of the observed infections could be explained by wind-borne transmission up to 25 km (15.5 miles)(16). Another case control study determined that ILT case flocks were 9.9 times more likely to be located within the wind vector of a clinical ILT flock during the 14-day incubation period compared with control flocks (7). Although highly dependent on variable conditions, these findings indicate that backyard flocks could bridge the gap between flocks by facilitating disease transmission during an outbreak, especially in a poultry-dense location. Based on our results, the level of biosecurity used in backyard flocks could use some improvement. Although free range has humane benefits, exposures to wild birds, waterfowl, and pests increase the risk of disease transmission to and within a flock. They also increase the likelihood of flock owners’ exposure to zoonotic diseases as almost two thirds never wear designated clothing, which may carry pathogens. Several backyard flock owners maintained a variety of species on their premises; however, 30% did not keep them separate, a good practice for preventing disease as some species may carry disease without any signs of illness. Although more than half (56.1%) of owners also reported observing signs of disease in their flock within the past 6 mo, only 14.6% sought diagnostic laboratory help, indicating that owners may be unaware of these services or feel that the diseases are not significant. However, disease surveillance of this population relies heavily on the voluntary reporting of clinical disease that, if left unreported, could allow disease organisms to incubate for several weeks within a flock. Although this study’s findings may not be generalized to the total backyard flock population, they do contribute to the ever-evolving knowledge on backyard flocks and the dynamics of disease transmission. One limitation of this study was the relatively poor response rate of 4.1%; however, it is believed to stem from the concern over the mandatory reporting of disease from another unpublished study. Secondary mailings that may have improved the survey sample size were not conducted. The study population also was limited to registered Maryland flocks, a convenience sampling method that may result in selection bias and therefore not be representative of the true sample population. It is evident based on the findings of this study that biosecurity education in noncommercial flocks should be promoted and is a
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necessary step toward disease prevention, especially as many of the owners are relatively new to backyard poultry (#5 yr). Although many studies have identified associations with certain management practices, this study evaluated owner and flock demographics and flock management practices, including husbandry, human-to-bird interaction, bird exposure risks, poultry health status, and biosecurity. These data have provided important information on what backyard flock owners are actually practicing so that policy development and future educational programs can focus on these areas, fill the knowledge gaps, and further mitigate the spread of disease. REFERENCES 1. Beard, C. W. It is like a ticking bomb. News and views. U.S. Poultry & Egg Association, Tucker, GA. 2010. 2. Brooks, J. 2004 Avian influenza Delmarva interagency cooperation. In: Proc. 39th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 17–19. 2005. 3. [CDC] Centers for Disease Control and Prevention. Past avian influenza outbreaks. [Internet]. [modified 2006 Feb 17; cited 2012 Sep 3]. Available from: http://www.cdc.gov/flu/avian/outbreaks/past.htm 4. CDC. Past outbreaks of avian influenza in North America [Internet]. [modified 2012 Jun 21; cited 2012 Sep 3]. Available from: http://www.cdc. gov/flu/avianflu/past-outbreaks.htm 5. Delmarva Poultry Industry, Inc. Facts about Maryland’s broiler chicken industry (2010). [Internet]. [cited 2012 Sep 3]. Available from: www.dpichicken.org/faq_facts/docs/factsmd2010.doc 6. Gaffga, N. H., C. B. Behravesh, P. J. Ettestad, C. B. Smelser, A. R. Rhorer, A. B. Cronquist, N. A. Comstock, S. A. Bidol, N. J. Patel, P. Gerner-Smidt, W. E. Keene, T. M. Gomez, B. A. Hopkins, M. J. Sotir, and F. J. Angulo. Outbreak of salmonellosis linked to live poultry from a mailorder hatchery. N. Engl. J. Med. 366:2065–2073. 2012. 7. Johnson, Y., N. Gedamu, M. Colby, M. Myint, S. Steele, M. Salem, and N. Tablante. Wind-borne transmission of infectious laryngotracheitis between commercial poultry operations. Int. J. Poult. Sci. 4:263–267. 2005. 8. [MDA] Maryland Department of Agriculture. 2012 Fair and show requirements. [Internet]. [cited 2013 Mar 4]. Available http://mda. maryland.gov/animalHealth/Pages/fairs-poultry.aspx 9. MDA. Maryland poultry premises registration. [Internet]. [cited 2013 Mar 4]. Available from: http://mda.maryland.gov/animalHealth/ Forms2/poultry_registration.pdf 10. Medina, R., and A. Garcia-Sastre. Influenza A viruses: new research developments. Nat. Rev. 9:590–603. 2011. 11. Nespeca, R., J. Vaillancourt, and W. E. Morrow. Validation of a poultry biosecurity survey. Prev. Vet. Med. 31:73–86. 1997.
12. Shane, S. M. Preventing erosive diseases in broiler parents. Zootech. Int. 16:58–60. 1993. 13. Sims, L. D., J. Domenech, C. Benigno, S. Kahn, A. Kamata, J. Lubroth, V. Martin, and R. Roeder. Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet. Rec. 157:159–164. 2005. 14. Smeltzer, M. A. Delmarva avian influenza epidemiology. In: Proc. 39th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 43–44. 2005. 15. Smith, E., J. Reif, A. Hill, K. Slota, R. Miler, Kathe Bjork, and K. Pabilona. Epidemiologic characterization of Colorado backyard bird flocks. Avian Dis. 56:263–271. 2012. 16. Ssematimba, A., T. Hagenaars, and M. de Jong. Modeling the windborne spread of highly pathogenic avian influenza virus between farms. PLoS ONE 7:e31114. 2012. 17. Tablante, N., M. San Myint, Y. Johnson, K. Rhodes, M. Colby, and G. Hohenhaus. A survey of biosecurity practices as risk factors affecting broiler performance on the Delmarva Peninsula. Avian Dis. 46:730–734. 2002. 18. USDA. Part I: Reference of health and management of backyard/ small production flocks in the United States, 2004. [modified 2013 Feb 15; cited 2012 Sep 3]. Available from: http://www.aphis.usda.gov/animal_ health/nahms/poultry/downloads/poultry04/Poultry04_dr_PartI.pdf 19. [USDA] U.S. Department of Agriculture. Poultry 2010. Reference of the health and management of chicken flocks in urban settings in four U.S. cities, 2010. U.S. Department of Agriculture-Animal and Plant Health Inspection Service-Veterinary Services, Centers for Epidemiology and Animal Health, Fort Collins, CO. 2011. 20. Vaillancourt, J., A. Martinez, C. Smith, and D. Ley. The epidemiology of Mycoplasma gallisepticum in North Carolina. In: Proc. 35th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 34–36. 2000. 21. [WHO] World Health Organization. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. [Internet]. [modified 2013 Feb 15; cited 2012 Sep 3]. Available from: http:// www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_ archives/en/index.html 22. Yendell, S., I. Rubinoff, D. Lauer, J. Bender, and J. Scheftel. Antibody prevalence of low pathogenicity avian influenza and evaluation of management practices in Minnesota backyard poultry flocks. Zoonoses Public Health 59:139–143. 2012.
ACKNOWLEDGMENTS We thank all those at the MDA who helped make this project possible as well as the Maryland backyard flock owners who participated in this study. This project was funded by the Maryland Agricultural Experiment Station Competitive Grants Program.
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AVIAN DISEASES 57:233–237, 2013
Evaluation of Maryland Backyard Flocks and Biosecurity Practices Jennifer M. Madsen,A Nickolas G. Zimmermann,B Jennifer Timmons,C and Nathaniel L. TablanteAD A
Virginia-Maryland Regional College of Veterinary Medicine, University of Maryland, College Park, MD 20742 B Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742 C Department of Agriculture, Food and Resource Sciences, University of Maryland Eastern Shore, Princess Anne, MD 21853 Received 21 October 2012; Accepted 7 February 2013; Published ahead of print 11 February 2013 SUMMARY. Domesticated poultry are susceptible to infectious and zoonotic diseases and can serve as a transmission source to other bird and human populations. In recent years, the number of noncommercial poultry has been on the rise in the United States. To evaluate potential risks of this growing population, a descriptive epidemiologic survey was conducted among Maryland backyard flocks. Owner and flock demographics were characterized as well as management practices such as husbandry, human-tobird interaction, bird exposure risks, poultry health status, and biosecurity. Data from the 41 returned questionnaires indicated a median flock size of 38 birds (range, 3–901). Chickens accounted for 86.5% of the reported birds overall. Just over half of the owners (51.2%) kept chickens only, with the remaining backyard flocks consisting of chickens, other gallinaceous species, waterfowl, or a combination. Of flocks with multiple species, 70.0% of owners did not keep them separate. Almost two thirds of owners (61.0%) had kept poultry for #5 yr, with 44.0% of all flocks on free range. Over the past 2 yr, predation was the highest cause of specific mortality (57.1%) followed by disease (30.2%), unknown (8.7%), and injury (4.0%), and over half of owners (56.1%) reported signs of disease in their flock within the last 6 mo. Biosecurity practices were highly variable among flocks. Data from this study identified gaps in the disease prevention and biosecurity practices of backyard flocks. These results can be useful in developing educational extension and outreach programs as well as policies, in efforts to further mitigate the spread of diseases. RESUMEN. Evaluacio´n de las parvadas de traspatio en el estado de Maryland y de sus pra´cticas de bioseguridad. Las aves dome´sticas son susceptibles a las enfermedades infecciosas y zoono´ticas y pueden servir como una fuente de transmisio´n a otras aves y a poblaciones humanas. En an˜os recientes, el taman˜o de la avicultura no comercial ha ido en aumento en los Estados Unidos. Para evaluar los riesgos potenciales de esta poblacio´n en crecimiento, se llevo´ a cabo un estudio epidemiolo´gico descriptivo en parvadas de traspatio de Maryland. La demografı´a de las parvadas y de los propietarios fue caracterizada ası´ como las pra´cticas de manejo, tales como el manejo de crianza, la interaccio´n entre aves y humanos, los riesgos de exposicio´n de las aves, el estado de salud de las aves y su bioseguridad. Los datos de los 41 cuestionarios indicaron un taman˜o de parvada promedio de 38 aves (rango, de tres a 901 aves). Los pollos representaron el 86.5% de las aves reportadas en general. Un poco ma´s de la mitad de los propietarios (51.2%) mantuvo pollos solamente, mientras que las parvadas restantes consistieron de pollos, de otras especies de gallina´ceas, aves acua´ticas, y sus combinaciones. De las parvadas con mu´ltiples especies, el 70.0% de los propietarios no mantuvieron las diferentes especies alojadas por separado. Casi dos tercios de los propietarios (61.0%) habı´an mantenido aves de corral por ma´s de cinco an˜os, con un 44.0% de las parvadas mantenidas en pastoreo. En los dos u´ltimos an˜os, la depredacio´n fue la mayor causa de mortalidad especı´fica (57.1%) seguida por enfermedades (30.2%), por causas no determinadas (8.7%) y por lesiones (4.0%), y ma´s de la mitad de los propietarios (56.1%) informaron la presencia de signos de enfermedad en sus parvadas en los u´ltimos seis meses. Las pra´cticas de bioseguridad fueron muy variables entre las parvadas. Los datos de este estudio identificaron deficiencias en la prevencio´n de enfermedades y en las pra´cticas de bioseguridad en las parvadas de traspatio. Estos resultados pueden ser u´tiles para el desarrollo de programas educativos y de extensio´n, ası´ como para las polı´ticas y esfuerzos para disminuir la diseminacio´n de las enfermedades. Key words: backyard flock, biosecurity, epidemiology, zoonotic disease, poultry, risk factors, avian influenza, education Abbreviations: AI 5 avian influenza; HPAI 5 highly pathogenic avian influenza; ILT 5 infectious laryngotracheitis; LPAI 5 low pathogenic avian influenza; MDA 5 Maryland Department of Agriculture; MG 5 Mycoplasma gallisepticum; NAHMS 5 National Animal Health Monitoring System; USDA 5 U.S. Department of Agriculture
Backyard flock ownership is growing in popularity across the United States from country farms to urban residences, and as the numbers of unregulated poultry increase, so does the need for disease surveillance and biosecurity education (19). Domesticated poultry are susceptible to infectious and zoonotic diseases and can serve as transmission sources to other bird and human populations (6,10,13). In recent years, some states, including Maryland, have begun taking an active approach to surveillance by requiring flock registration and testing before participating in fair or auction markets, operating hatcheries, or selling local eggs or poultry (8). However, this population only accounts for a small percentage of owners based on the U.S. Department of Agriculture (USDA), National Animal Health Monitoring System (NAHMS) 2004 survey that reported that only 11.2% of owners ranked these D
Corresponding author. E-mail: [email protected]
categories (extra income and clubs/social interactions) as high and very high as primary reasons for keeping poultry (18). Poultry can carry a variety of infectious diseases of economic importance, and they are capable of subclinically harboring human pathogens. This capability warrants consideration in backyard flocks because biosecurity practices are generally not monitored or enforced. Salmonella poisoning in recent years has been linked to contact with contaminated poultry. From 2004 to 2011, 316 cases of Salmonella Montevideo from 43 states were reported to be the result of handling infected chicks, ducklings, and live poultry (6). Avian influenza (AI) virus is another major pathogen of concern that can cause mild-to-severe respiratory disease in gallinaceous species. It also is capable of causing disease in humans, although rare. Low pathogenic AI (LPAI) and highly pathogenic AI (HPAI) viruses have been responsible for the culling of millions of birds worldwide, costing billions in containment and production losses. In 2004, an
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Table 1. Backyard flock species distribution and median flock size among the surveyed regions of Maryland. Northern Maryland
No. of flocks Median flock size SpeciesB Chickens Turkeys Ducks Guinea fowl Pheasants Geese Peacocks Chuckers Doves Total
Southern Maryland
Eastern Shore
Overall (%)
20 40
12 32
9 42
41 38
2174 216 38 50 0 13 4 0 3 2498
328 8 107 33 33 2 6 3 0 520
1173 35 12 0 0 9 0 0 0 1229
3675 259 157 83 33 24 10 3 3 4247
RangeA
3–901
(86.5) (6.1) (3.7) (2.0) (0.8) (0.6) (0.2) (0.07) (0.07)
3–901 0–210 0–65 0–25 0–30 0–8 0–6 0–3 0–3
A B
Number of birds per flock. Total number of birds by species.
LPAI H7N2 outbreak hit Maryland and Delaware and resulted in the costly depopulation of 378,000 and 84,000 chickens, respectively (2,14). Although no human cases of AI were reported, transmission of influenza A viruses from poultry to people has been documented previously in North America (3,4). These cases were treatable and made a full recovery; however, in other parts of the world, the HPAI H5N1 strain has caused 607 human cases and 358 deaths, resulting in an extremely high case fatality rate (10,13,21). Transmission of AI viruses through trade of infected poultry and contaminated equipment is considered one of the main means of spread, but with the use of biosecurity, the risk of introducing disease can be prevented or reduced (11,12,13). In an effort to control the transmission of poultry diseases, some U.S. states require all poultry owners to register flocks with their state’s department of agriculture. In 2005, the Maryland General Assembly passed legislation mandating backyard poultry registration. As of June 2011, there have been 3258 backyard flocks registered with the Maryland Department of Agriculture (MDA) (9). Understanding backyard flock management practices has economic importance as well. Five counties in Maryland lead the nation in broiler production. According to 2010 Delmarva Poultry Industry, Inc. data, Somerset County ranked 25th, Worcester County 26th, Wicomico County 36th, Caroline County 40th, and Dorchester County 63rd among all U.S. counties (5). This study aimed to characterize Maryland backyard poultry and to identify gaps in biosecurity practices in an effort to develop better education programs and healthier flocks. MATERIALS AND METHODS Study design. Survey locations were divided into three regions of Maryland by counties: Northern (Frederick and Carroll), Southern (St. Mary’s and Charles), and Eastern Shore (Caroline, Dorchester, Talbot, Wicomico, and Worcester). County selection was based on the high proportion of registered backyard flock owners as well as relative location to commercial industries and auction markets. In May 2011, the MDA confidentially mailed 1000 informational letters and return postcards to poultry owners enrolled in the Maryland Poultry Registration Program. Backyard flocks were defined using the NAHMS Poultry 2004 guidelines as residences with fewer than 1000 birds (other than pet birds or in addition to pet birds). If poultry owners wished to participate, they were asked to contact the University of Maryland via email or via prepaid return postcards.
Participants were eligible for the study if they lived within Maryland, owned domesticated fowl, and had a flock size fewer than 1000 birds. Respondents were offered a free diagnostic health status report of their flock as an incentive to participate in the study. Upon agreement to participate, owners were sent an information sheet, questionnaire, and consent form providing further details of the study, including the risks and benefits of participation. This study was approved in accordance with the University of Maryland’s Institutional Review Board (110335) and Federal Policy for the Protection of Human Subjects (45 CFR 46). Questionnaire. A four-page questionnaire, adapted from USDA Poultry 2010 and previous publication by Tablante et al. was created to determine biosecurity factors that may be associated with the health status of small flocks (17,18,19). Upon state and academic review by the Maryland state veterinarian, assistant state veterinarians, one animal health inspector from the MDA, and poultry extension agents with the University of Maryland, a questionnaire and information sheet were mailed to backyard flock owners who agreed to participate. Participants were asked to self-report information on the number and species of poultry reared, presence of other animals, animal husbandry, opportunities for interaction between wild birds and poultry, flock biosecurity measures, and health status of poultry. The questionnaire is available upon request.
RESULTS
Backyard flock demographics. Of the 1000 contacted backyard flock owners, 41 (4.1%) agreed to participate and all completed surveys. From the returned surveys, we determined that flock sizes ranged from three to 901 birds, with the median of 38 birds per flock. All owners reported having chickens on their property, with just over half (51.2%) having chickens as the only species of domestic poultry. Chickens accounted for 86.5% of the reported birds overall (Table 1). The remaining flocks had a mix of chickens and other domestic bird species, with 17.1% keeping chickens and turkeys; 24.4% raising chickens and waterfowl; 9.8% keeping chickens, turkeys, and waterfowl; and 14.6% having chickens, waterfowl, and game fowl species on the property. Only two flocks had peafowl (Pavo spp.), with one peafowl flock also having chickens, turkeys, waterfowl, and game fowl. The number of species in a flock ranged from one to six, with the median count of one. Sixty-one percent of surveyed owners have kept backyard poultry for #5 yr, whereas 24.4% have had poultry between 6 and 10 yr and 14.6% have kept poultry for .10 yr. The predominant reason for keeping poultry was personal consumption of eggs (56.1%),
Biosecurity in Maryland backyard flocks
Table 2. Percentage of backyard flock characteristics as reported by flock owners. Characteristic
%
Flocks with multiple species Chickens and turkeys Chickens and waterfowlA PoultryB and waterfowlA PoultryB and peafowl (peacock) PoultryB and game fowlC Chickens, waterfowl,A and game fowlC
17.1 24.4 9.8 2.4 7.3 14.6
Duration of ownership #12 months 13 mo–5 yr 6–10 yr .10 yr
17.1 43.9 24.4 14.6
Reason for keeping birds Home egg consumption Selling eggs Selling live birds Pets Home meat consumption Selling meat
56.1 29.3 4.9 4.9 2.4 2.4
Causes of mortality (previous 2 yr) Predation Disease Unknown Injury
57.1 30.2 8.7 4.0
Signs of disease (previous 6 mo) Diarrhea Poor egg production (decrease in or soft or misshapen eggs) Respiratory (coughing, sneezing, nasal secretions, or swollen sinuses) Weight loss or anorexia Neurologic (lack of coordination or weakness) Swelling (head, comb, wattles, or hocks) A
29.2 29.2 9.7 7.3 4.9 0.0
Waterfowl is defined as having ducks or geese. Poultry is defined as having both chickens and turkeys. C Game fowl is defined as having pheasant, guinea fowl, chucker, or doves. B
Fig. 1.
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followed by selling eggs (29.3%). Other owners kept poultry for live sale (4.9%), as pets (4.9%), for home consumption (2.4%), or to sell as meat (2.4%; Table 2). Flock management and exposures. Housing types for poultry was recorded as 39.0% cooped, fenced-in and covered; 17.0% cooped, fenced-in but not covered; 29.3% free range; and 14.7% free range near a water source such as ponds or streams. Of the 20 backyard flocks with multiple species, only six owners (30.0%) keep them separate. Owner and poultry exposure to other animals was variable. Overall, 53.7% of poultry were reported as accessible to wild birds whereas only 9.8% were reported as accessible to waterfowl (Fig. 1). Personal interaction with livestock, such as pigs, sheep, and cattle, was reported by 41.5% of owners, whereas 31.7% of the poultry populations were exposed to livestock. Only five of 41 (12.2%) flocks reported being within a quarter mile of a commercial flock, whereas 68.0% of owners reported being within a quarter mile of other backyard flocks. In the average year, 10 owners visited commercial poultry sites one to 12 times (median 5 7), with three owners coming into contact with commercial birds. In the average year, 10 owners also visited other backyard flocks one to 78 times (median 5 7.5), with nine owners coming into direct contact with birds. Nine owners did not allow visitors, and of those who permitted guests, 73.0% allowed direct contact with birds. Only 4.9% of owners sold birds at a market and 7.3% bought birds from markets. Within the last year, 83.0% of owners purchased new birds. Of those who purchased birds, 17.6% did not isolate them before introduction into the flock. Those who did isolate, on average, separated their new birds for 9–10 wk, with three owners keeping new birds separate indefinitely. Flocks originated from multiple sources, with some individual flock owners obtaining birds from several locations. Mail-order hatcheries were the predominant means of acquiring birds, with 30 owners using online-based hatcheries from other states. Nine owners used local retail feed and farm supply stores, whereas three flock owners purchased birds from commercial poultry houses and another three owners from a private source, such as a friend or from other backyard flocks. Four flock owners purchased birds from county fairs, flea markets, or bird auctions. Flock health. Only one of 41 owners vaccinated birds once they were on the premises. The owner vaccinated for Mycoplasma gallisepticum (MG), infectious laryngotracheitis (ILT) virus, and fowlpox. In the previous 2 yr, owners reported predation as having the highest cause-specific mortality rate (57.1%), followed by disease (30.2%), unknown (8.7%), and injury (4.0%; Table 2). Just over
Percentage of backyard flocks and owners with reported exposure to other animals.
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Table 3. Frequency (percentage) of biosecurity practices reported by backyard flock owners when interacting with flock. Biosecurity factor
Always
Sometimes
Never
Hand washing Designated clothes Dedicated footbath Dedicated footwear Visitor wash hands Visitor designated clothes
65.8 7.3 7.3 31.7 62.5 12.5
22.0 29.3 — — 15.6 3.1
12.2 63.4 92.7 68.3 21.9 84.4
half (56.1%) of owners also reported observing signs of disease in their flock within the past 6 mo. Almost one third (29.2%) of all owners recalled seeing birds with diarrhea, whereas another 29.2% reported a decrease in egg production or soft or misshapen eggs. A few reported respiratory disease symptoms (9.7%), such as coughing, sneezing, nasal secretions, or swollen sinuses, and 7.3% observed weight loss or decreased appetite in their flock. Two owners reported neurologic signs (4.9%) such as lack of coordination or weakness. No owners had birds with swelling of the head, comb, wattles, or hocks. Six backyard flock owners (14.6%) reported that they have previously sent an ill bird to a diagnostic laboratory. Biosecurity practices. For sanitation and decontamination, only three of the owners (7.3%) routinely use a footbath at the entrance to their poultry premises, and two of these three owners also use dedicated footwear. Of the remaining owners, 11 wear a different pair of shoes when entering their poultry area. Although the majority of owners (65.8%) always wash their hands before and after handling their birds, many (63.4%) never wear dedicated clothing (Table 3). More than two thirds of owners clean and disinfect housing and equipment (68.3%), and all but one owner disposes of litter by means of composting (47.4%), setting in a manure pile (31.6%), spreading on fields (18.4%), or having it hauled away (2.6%). Dead birds were usually buried on site (43.6%), composted (20.5%), thrown in trash (15.4%), hauled away (10.3%), or fed to other animals (10.2%). Pest control such as mouse traps or insecticides were used in 39.0% of backyard flock premises. DISCUSSION
Backyard flocks play a role in the ecology and transmission pathways of diseases. However, information on this population remains limited and often presents with unique challenges due to lack of registration databases or flock owner reporting. This study aimed to describe Maryland backyard flocks and to evaluate current management practices. Despite the poor response rate, the results of this study are important as only a handful of other studies have assessed U.S. backyard flock communities with which this study finds both similarities and differences. Several factors may contribute to observed differences between studies, including sample size, climate, population density, culture, state and county regulations, and biosecurity education. A recent cross-sectional study characterizing Colorado backyard flocks also found chickens as the predominant species that were primarily kept for personal consumption (meat and eggs). The Colorado survey found 34.1% of flocks to be free range, whereas 44.0% of surveyed Maryland flocks were reported free range. Among surveyed Maryland flocks, 82.4% reported isolating new birds before introduction into the flock, whereas only 59.9% of sampled Colorado flock owners quarantined new birds (15). However, a Minnesota study found that 82.9% of backyard flock owners separated new birds as well (22).
Unlike the previous reports, this study evaluated the length of ownership to estimate the rate of new flock owners in Maryland; the findings implied that ownership of backyard poultry is on the rise. With the increase in numbers of new flock owners, greater efforts for education on disease prevention are necessary. Almost half of flock owners visited other backyard flocks or commercial poultry sites and several allowed visitors onto their poultry premises. This increase in flock traffic potentially increases the risk of introducing disease via fomites as visitors’ vehicles, boots, and clothing may carry pathogens. Several outbreak investigations have linked fomites in connection with disease spread, such as the 1983 HPAI outbreak in commercial poultry that was associated with human and equipment traffic from New York live bird markets (1). Another study found an association between farms of the 1999 MG outbreak in North Carolina as a poultry grower returned to his flock after visiting an MG-positive farm without changing his contaminated clothing or footwear (20). Although the other half of backyard flock owners did not visit other poultry premises, the proximity of backyard flocks to each other and commercial poultry houses could potentially increase the chances of disease spread. One study designed a model to predict the potential wind-borne transmission of HPAI virus particles between farms given the conditions of the 2003 HPAI outbreak in the Netherlands. The study estimated that 24.0% of the observed infections could be explained by wind-borne transmission up to 25 km (15.5 miles)(16). Another case control study determined that ILT case flocks were 9.9 times more likely to be located within the wind vector of a clinical ILT flock during the 14-day incubation period compared with control flocks (7). Although highly dependent on variable conditions, these findings indicate that backyard flocks could bridge the gap between flocks by facilitating disease transmission during an outbreak, especially in a poultry-dense location. Based on our results, the level of biosecurity used in backyard flocks could use some improvement. Although free range has humane benefits, exposures to wild birds, waterfowl, and pests increase the risk of disease transmission to and within a flock. They also increase the likelihood of flock owners’ exposure to zoonotic diseases as almost two thirds never wear designated clothing, which may carry pathogens. Several backyard flock owners maintained a variety of species on their premises; however, 30% did not keep them separate, a good practice for preventing disease as some species may carry disease without any signs of illness. Although more than half (56.1%) of owners also reported observing signs of disease in their flock within the past 6 mo, only 14.6% sought diagnostic laboratory help, indicating that owners may be unaware of these services or feel that the diseases are not significant. However, disease surveillance of this population relies heavily on the voluntary reporting of clinical disease that, if left unreported, could allow disease organisms to incubate for several weeks within a flock. Although this study’s findings may not be generalized to the total backyard flock population, they do contribute to the ever-evolving knowledge on backyard flocks and the dynamics of disease transmission. One limitation of this study was the relatively poor response rate of 4.1%; however, it is believed to stem from the concern over the mandatory reporting of disease from another unpublished study. Secondary mailings that may have improved the survey sample size were not conducted. The study population also was limited to registered Maryland flocks, a convenience sampling method that may result in selection bias and therefore not be representative of the true sample population. It is evident based on the findings of this study that biosecurity education in noncommercial flocks should be promoted and is a
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necessary step toward disease prevention, especially as many of the owners are relatively new to backyard poultry (#5 yr). Although many studies have identified associations with certain management practices, this study evaluated owner and flock demographics and flock management practices, including husbandry, human-to-bird interaction, bird exposure risks, poultry health status, and biosecurity. These data have provided important information on what backyard flock owners are actually practicing so that policy development and future educational programs can focus on these areas, fill the knowledge gaps, and further mitigate the spread of disease. REFERENCES 1. Beard, C. W. It is like a ticking bomb. News and views. U.S. Poultry & Egg Association, Tucker, GA. 2010. 2. Brooks, J. 2004 Avian influenza Delmarva interagency cooperation. In: Proc. 39th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 17–19. 2005. 3. [CDC] Centers for Disease Control and Prevention. Past avian influenza outbreaks. [Internet]. [modified 2006 Feb 17; cited 2012 Sep 3]. Available from: http://www.cdc.gov/flu/avian/outbreaks/past.htm 4. CDC. Past outbreaks of avian influenza in North America [Internet]. [modified 2012 Jun 21; cited 2012 Sep 3]. Available from: http://www.cdc. gov/flu/avianflu/past-outbreaks.htm 5. Delmarva Poultry Industry, Inc. Facts about Maryland’s broiler chicken industry (2010). [Internet]. [cited 2012 Sep 3]. Available from: www.dpichicken.org/faq_facts/docs/factsmd2010.doc 6. Gaffga, N. H., C. B. Behravesh, P. J. Ettestad, C. B. Smelser, A. R. Rhorer, A. B. Cronquist, N. A. Comstock, S. A. Bidol, N. J. Patel, P. Gerner-Smidt, W. E. Keene, T. M. Gomez, B. A. Hopkins, M. J. Sotir, and F. J. Angulo. Outbreak of salmonellosis linked to live poultry from a mailorder hatchery. N. Engl. J. Med. 366:2065–2073. 2012. 7. Johnson, Y., N. Gedamu, M. Colby, M. Myint, S. Steele, M. Salem, and N. Tablante. Wind-borne transmission of infectious laryngotracheitis between commercial poultry operations. Int. J. Poult. Sci. 4:263–267. 2005. 8. [MDA] Maryland Department of Agriculture. 2012 Fair and show requirements. [Internet]. [cited 2013 Mar 4]. Available http://mda. maryland.gov/animalHealth/Pages/fairs-poultry.aspx 9. MDA. Maryland poultry premises registration. [Internet]. [cited 2013 Mar 4]. Available from: http://mda.maryland.gov/animalHealth/ Forms2/poultry_registration.pdf 10. Medina, R., and A. Garcia-Sastre. Influenza A viruses: new research developments. Nat. Rev. 9:590–603. 2011. 11. Nespeca, R., J. Vaillancourt, and W. E. Morrow. Validation of a poultry biosecurity survey. Prev. Vet. Med. 31:73–86. 1997.
12. Shane, S. M. Preventing erosive diseases in broiler parents. Zootech. Int. 16:58–60. 1993. 13. Sims, L. D., J. Domenech, C. Benigno, S. Kahn, A. Kamata, J. Lubroth, V. Martin, and R. Roeder. Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet. Rec. 157:159–164. 2005. 14. Smeltzer, M. A. Delmarva avian influenza epidemiology. In: Proc. 39th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 43–44. 2005. 15. Smith, E., J. Reif, A. Hill, K. Slota, R. Miler, Kathe Bjork, and K. Pabilona. Epidemiologic characterization of Colorado backyard bird flocks. Avian Dis. 56:263–271. 2012. 16. Ssematimba, A., T. Hagenaars, and M. de Jong. Modeling the windborne spread of highly pathogenic avian influenza virus between farms. PLoS ONE 7:e31114. 2012. 17. Tablante, N., M. San Myint, Y. Johnson, K. Rhodes, M. Colby, and G. Hohenhaus. A survey of biosecurity practices as risk factors affecting broiler performance on the Delmarva Peninsula. Avian Dis. 46:730–734. 2002. 18. USDA. Part I: Reference of health and management of backyard/ small production flocks in the United States, 2004. [modified 2013 Feb 15; cited 2012 Sep 3]. Available from: http://www.aphis.usda.gov/animal_ health/nahms/poultry/downloads/poultry04/Poultry04_dr_PartI.pdf 19. [USDA] U.S. Department of Agriculture. Poultry 2010. Reference of the health and management of chicken flocks in urban settings in four U.S. cities, 2010. U.S. Department of Agriculture-Animal and Plant Health Inspection Service-Veterinary Services, Centers for Epidemiology and Animal Health, Fort Collins, CO. 2011. 20. Vaillancourt, J., A. Martinez, C. Smith, and D. Ley. The epidemiology of Mycoplasma gallisepticum in North Carolina. In: Proc. 35th National Meeting on Poultry Health and Processing, Ocean City, MD. pp. 34–36. 2000. 21. [WHO] World Health Organization. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. [Internet]. [modified 2013 Feb 15; cited 2012 Sep 3]. Available from: http:// www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_ archives/en/index.html 22. Yendell, S., I. Rubinoff, D. Lauer, J. Bender, and J. Scheftel. Antibody prevalence of low pathogenicity avian influenza and evaluation of management practices in Minnesota backyard poultry flocks. Zoonoses Public Health 59:139–143. 2012.
ACKNOWLEDGMENTS We thank all those at the MDA who helped make this project possible as well as the Maryland backyard flock owners who participated in this study. This project was funded by the Maryland Agricultural Experiment Station Competitive Grants Program.
