A Framework to Reduce Infectious Disease Risk from Urban Poultry in the United States

Abstract

Objectives

Backyard poultry ownership is increasingly common in U.S. cities and is regulated at the local level. Human contact with live poultry is a well-known risk for infection with zoonotic pathogens, notably Salmonella, yet the ability of local jurisdictions to reduce the risk of infectious disease transmission from poultry to humans is unstudied. We reviewed urban poultry ordinances in the United States and reported Salmonella outbreaks from backyard poultry to identify regulatory gaps in preventing zoonotic pathogen transmission. Based on this analysis, we propose regulatory guidelines for U.S. cities to reduce infectious disease risk from backyard poultry ownership.

Methods

We assessed local ordinances in the 150 most populous U.S. jurisdictions for content related to noncommercial poultry ownership using online resources and communications with government officials. We also performed a literature review using publicly available data sources to identify human infectious disease outbreaks caused by contact with backyard poultry.

Results

Of the cities reviewed, 93% (n=139) permit poultry in some capacity. Most urban poultry ordinances share common characteristics focused on reducing nuisance to neighbors. Ordinances do not address many pathways of transmission relevant to poultry-to-human transmission of pathogens, such as manure management.

Conclusions

To reduce the risk of pathogen exposure from backyard poultry, urban ordinances should incorporate the following seven components: limited flock size, composting of manure in sealed containers, prohibition of slaughter, required veterinary care to sick birds, appropriate disposal of dead birds, annual permits linked to consumer education, and a registry of poultry owners.

Backyard poultry ownership in urban areas of the United States has increased dramatically in recent decades, and approximately 50 million chicks are sold annually in the United States.^1–3 Human contact with live poultry is a well-documented risk factor for infection with zoonotic pathogens, including Salmonella species (spp.), Listeria spp., Campylobacter spp., extraintestinal pathogenic Escherichia coli, Enterococcus spp., and avian influenza viruses.^4–6 Poultry ownership is regulated at the municipal level, typically in the context of an urban agriculture ordinance. Despite the growing popularity of urban poultry keeping, little research to date has systematically evaluated urban poultry ordinances for their ability to reduce infectious disease transmission from poultry to humans.

Across the country, urban ordinances excluding livestock from cities emerged in the early 1900s in response to sanitation problems, increasing awareness of disease risk, and noise and odor concerns.^7–9 Beginning in the 1950s, the intensification of animal agriculture in the United States increased production of meat products in rural areas and reduced the cost of meat at the market, eliminating the need for livestock ownership in the city.¹⁰ In the early 2000s, Madison, Wisconsin, and Seattle, Washington, were among the first U.S. cities to reintroduce poultry ownership as a regulated activity within the city. This practice quickly spread, and as of 2014, approximately 700 U.S. jurisdictions allowed limited chicken ownership as a regulated activity, according to community postings on a popular website, backyardchickens.com.¹¹ Motivations behind urban poultry ownership include hobby, increased control of food choices, education for children, improved nutrition, and benefits for the environment and animal welfare.^12,13

The poultry breeding industry that supplies noncommercial chicks for urban poultry holders is highly centralized, with fewer than 20 hatcheries supplying poultry to the backyard market nationwide.¹⁴ These hatcheries supply chicks to local feed stores, which in turn sell them to consumers and also sell directly to consumers through online purchasing and shipment to the household (Figure 1). Some hatcheries breed and hatch chicks on site, while others serve as distributors of chicks bred at other facilities. Small-scale private sellers also offer chicks for sale and may advertise online, through flyers, or by word of mouth.

Figure 1.

Depiction of chick distribution network and pathways of pathogen transmission from poultry to humans in the context of backyard poultry ownership

Annually, an estimated 1.4 million people in the United States are infected with nontyphoidal Salmonella serovars; roughly 12% of these infections result in visits to physicians, 1% result in hospitalizations, and nearly 0.03% result in death.¹⁵ In the United States, exposure to noncommercial live poultry and eggs has been the source of 45 documented Salmonella outbreaks since 1991, with 1,581 documented illnesses, 221 hospitalizations, and five deaths.^4,16 Because the majority of gastrointestinal illnesses go unreported, the mortality and morbidity associated with Salmonella outbreaks from contact with noncommercial live poultry likely represent a small portion of the actual burden caused by this exposure.¹⁷

Despite these risks, many backyard poultry owners are unaware of infectious disease risks from poultry contact and do not engage in appropriate hygienic behaviors. A 2010 U.S. Department of Agriculture study suggested that more than 50% of urban poultry owners were unaware that live poultry contact poses infectious disease risks for humans, and nearly 25% reported not washing hands after handling live poultry.¹² Furthermore, antibiotics are available directly to consumers for purchase at feed stores without a prescription, in therapeutic form or as a component of poultry feed. The use of antibiotics for nontherapeutic purposes in food animal production poses risks for increased antibiotic resistance in human clinical medicine.^18,19 The scale, frequency, and public health implications of antibiotics in backyard poultry flocks remain largely unstudied.

We evaluated the characteristics of municipal ordinances guiding urban backyard poultry production in the United States. We reviewed the existing literature on the documented infectious disease outbreaks resulting from human contact with backyard poultry to identify transmission pathways of concern in the U.S. urban context. We identified gaps in current regulatory structure and provide a regulatory framework to reduce the risk of infectious disease transmission associated with this emerging practice.

METHODS

We evaluated local ordinances in the 150 largest urban U.S. jurisdictions, as ranked by 2013 population according to the U.S. Census, for content regarding noncommercial poultry ownership.²⁰ We used online resources and in-person communications (e.g., phone, e-mail, and in-person interviews) with city officials to collect and confirm data. We initially identified Web links to the municipal ordinances for poultry ownership through the website backyardchickens.com, where data from more than 1,000 ordinances have been compiled by users. We then verified data through independent searches of these ordinances online and through communications with local government officials. We performed Google searches for cities not included in the database. Three researchers gathered data during a 12-month period from June 2013–June 2014 and entered the data into a Microsoft^® Excel^® spreadsheet for analysis. Individuals involved in data collection and organization were trained in the use of standardized data entry procedures.

We performed a literature search to identify reported human infectious disease outbreaks and infections caused by contact with noncommercial poultry in the United States. We used databases (e.g., PubMed, Google Scholar, PLoS One, Web of Science, and Science Direct) and relevant keywords (e.g., “live poultry,” “zoonoses,” “urban poultry,” and “backyard poultry”) to locate outbreak reports and appropriate articles. In addition, the Centers for Disease Prevention and Control (CDC) publishes reports on Salmonella outbreaks in the United States, some of which have been attributed to contact with live poultry. These reports were also reviewed and incorporated into the analysis.

RESULTS

Regulation of urban poultry ownership

Of the 150 largest U.S. cities, 11 banned poultry and other livestock (i.e., Detroit, Michigan; Miami, Florida; Yonkers, New York; Bismarck, North Dakota; and Worcester, Massachusetts). The remaining jurisdictions (n=139) had current livestock ownership ordinances that were included in this analysis.

The ordinances we reviewed share a set of common characteristics, including maximum flock size; lot, coop, and sanitation restrictions; bans on rooster keeping, excessive noise, and odors; stipulations regarding veterinary care, animal slaughter, and disposal; permitting requirements; and owner education (Table 1).

Table 1.

Characteristics of selected U.S. urban poultry ordinances, 2014

sq. = square

ft. = feet

Flock size.

Seventy-five percent (n=103) of reviewed urban poultry ordinances specified a limit on the number of chickens allowed (ranging from four in San Francisco, California, to 25 in Atlanta, Georgia). Twelve percent (n=17) of municipalities, including Charlotte, North Carolina, and San Jose, California, regulate flock size by allowing a certain number of birds per acre or square footage of land. Cities also may specify that flock size is contingent on zoning areas within the city limits, with a reduced number of animals allowed in denser areas. Fewer than 5% of cities required permitting beyond a specific flock size, including St. Louis, Missouri, which allowed four chickens without a permit and eight with a permit (data not shown).

Lot, coop size, and sanitation.

Specifications regarding mandatory distances between an abutter's property and the coop or minimum required lot size were reported in nearly half (n=68) of reviewed ordinances. Distances between the coop and the street varied greatly by jurisdiction, from 5 to 350 feet. The median required distance between the coop and abutting residences was 50 feet. Sixty-three percent of ordinances (n=87) required design specifications for the coop itself. These restrictions included minimum square footage per bird, maximum height of the coop, and predator-proof structures. More than 50% of the ordinances (n=73) required adherence to basic sanitation requirements, such as ventilated coops, lime treatments, or designated bins for manure composting. Houston, Texas, and Charlotte, North Carolina, had stricter sanitation policies, requiring that coops be cleaned daily (data not shown).

Rooster keeping, noise, and odors.

Most cities (65%) banned roosters, although jurisdictions in the South and Southwest, including New Orleans, Louisiana, and Albuquerque, New Mexico, permitted roosters pending noise complaints. The policies that determine acceptable rooster ownership varied greatly by location. For example, while roosters were allowed in Los Angeles, California, if they are at least 100 feet from any neighbors, Louisville, Kentucky, allowed one rooster per property regardless of distance from abutters. Specifications regarding noise or odor were included in approximately one-third of ordinances. Most commonly, ordinances specified that poultry owners must abide by existing noise ordinances and that the coop not produce objectionable odors. The ordinance in Honolulu, Hawaii, has notably specific language in regard to noise, indicating that poultry may not make noise for more than 10 minutes at a time. Neighbor approval prior to permitting was unusual and was required by fewer than 5% of the cities evaluated, including Las Vegas, Nevada, and Minneapolis, Minnesota. Objections by a neighbor in Durham, North Carolina, on the basis of noise or odor can warrant an inspection of the property under question (data not shown).

Veterinary care, slaughter, and disposal.

Baltimore, Maryland, Austin, Texas, and Albuquerque, New Mexico, required poultry owners to provide veterinary care to sick birds, but such stipulations were unusual and only observed in these jurisdictions. With few exceptions, ordinances omitted specific language on animal slaughter, but restriction or prohibition was the norm when present.¹³ Boston, Massachusetts, and Chicago, Illinois, specifically forbade slaughter. Los Angeles allowed slaughtering, while San Francisco only allowed it when performed at a distance from the coop. Rochester, New York, required a poulterer's license for slaughtering, and Cleveland, Ohio, allowed for slaughter if the chicken was consumed on the premises. Policies for the disposal of dead birds were specified in fewer than 10% of ordinances (n=12) and varied significantly by jurisdiction. Bagging in the weekly trash, burying, composting, incineration, and dropping off at designated sites were the most commonly recommended and utilized methods (data not shown).

Permit requirements and owner education.

Permitting was required in 38% (n=52) of cities reviewed. Cities may charge a small fee to receive a permit, typically from $40–$60, with limited municipalities requiring permit renewal on an annual basis (Table 1). Inspections were occasionally required prior to approval; Charlotte, Richmond, Virginia, and Houston, Texas, required a property and coop inspection before a permit was granted. In Columbus, Ohio, and El Paso, Texas, veterinarians were responsible for inspecting properties and issuing permits, but such inspections were uncommon. In Jacksonville, Florida, permit applicants were required to attend an educational seminar hosted by the county's Agricultural Extension Office prior to receiving a permit. Richmond also had an educational component required alongside permitting. Such requirements were uncommon and not observed beyond these cities in our review (data not shown).

Zoonotic infections and backyard poultry

Salmonella is the only pathogen identified in reported human disease outbreaks associated with live, noncommercial poultry in the United States.¹⁶ The first reported Salmonella outbreak in the United States due to exposure to live, noncommercial poultry occurred in 1955.²¹ Since 1990, 45 reported Salmonella outbreaks have occurred in the United States from contact with live, noncommercial poultry.⁴ Table 2 details these Salmonella outbreaks.

Table 2.

Selected Salmonella outbreaks from contact with live, noncommercial poultry in the United States, 1990–2014

^aSvitlik C, Cartter M, McCarter Y, Hadler JL, Goeller D, Groves C, et al. Salmonella Hadar associated with pet ducklings—Connecticut, Maryland, and Pennsylvania, 1991. MMWR Morb Mortal Wkly Rep 1992;41(11):185-7.

^bBlythe D, Goldoft M, Lewis J, Stehr-Green P, Chehey R, Greenblatt J, et al. Salmonella serotype Montevideo infections associated with chicks—Idaho, Washington, and Oregon, spring 1995 and 1996. MMWR Morb Mortal Wkly Rep 1997;46(11):237-9.

^cBidol S, Stobierski MG, Robinson-Dunn B, Massey J, Hall W, Boulton M, et al. Salmonellosis associated with chicks and ducklings—Michigan and Missouri, spring 1999. MMWR Morb Mortal Wkly Rep 2000;49(14):297-9.

^dGaffga NH, Behravesh CB, Ettestad PJ, Smelser CB, Rhorer AR, Cronquist AB, et al. Outbreak of salmonellosis linked to live poultry from a mail-order hatchery. N Engl J Med 2012;366:2065-73.

^eBidol S, Stobierski M, Leschinsky D, Ettestad P, Smelser C, Sena-Johnson D, et al. Three outbreaks of Salmonellosis associated with baby poultry from three hatcheries—United States, 2006. MMWR Morb Mortal Wkly Rep 2007;56(12):273-6.

^fHedican E, Smith K, Jawahir S, Scheftel J, Kruger K, Birk R, et al. Multistate outbreaks of Salmonella infections associated with live poultry—United States, 2007. MMWR Morb Mortal Wkly Rep 2009;58(2):25-9.

^gLoharikar A, Briere E, Schwensohn C, Weninger S, Wagendorf J, Scheftel J, et al. Four multistate outbreaks of human Salmonella infections associated with live poultry contact, United States, 2009. Zoonoses Public Health 2012;59:347-54.

^hCenters for Disease Control and Prevention (US). Multistate outbreak of human Salmonella Hadar infections linked to live poultry in backyard flocks (final update). 2011 [cited 2014 Aug 12]. Available from: URL: http://www.cdc.gov/salmonella/hadar-live-poultry-07-12/index.html

ⁱCenters for Disease Control and Prevention (US). Multistate outbreak of human Salmonella Montevideo infections linked to live poultry in backyard flocks (final update). 2012 [cited 2014 Aug 12]. Available from: URL: http://www.cdc.gov/salmonella/montevideo-06-12/index.html

^jForshey TM, Nowicki S, Mohr M, Roney CS, Gomez TM, Mitchell JR, et al. Notes from the field: multistate outbreak of Salmonella Infantis, Newport, and Lille infections linked to live poultry from a single mail-order hatchery in Ohio—March–September 2012. MMWR Morb Mortal Wkly Rep 2013;62(11):213.

^kCenters for Disease Control and Prevention (US). Multistate outbreak of human Salmonella Typhimurium infections linked to live poultry in backyard flocks (final update). 2013 [cited 2014 Aug 4]. Available from: URL: http://www.cdc.gov/salmonella/typhimurium-live-poultry-04-13/index.html

^lCenters for Disease Control and Prevention (US). Multistate outbreak of human Salmonella infections linked to live poultry in backyard flocks, 2014 [cited 2014 Mar 3]. Available from: URL: http://www.cdc.gov/salmonella/live-poultry-05-14

S. = Salmonella

Recent outbreaks have been characterized by a diversity of Salmonella species, young age of cases (often <5 years of age), elevated severity of disease, and multistate distribution of cases. Since 2007, most reported outbreaks have been traced back to a hatchery that distributed infectious chicks to feed stores and/or directly to consumers.^22–30 Earlier outbreaks identified poultry contact as a risk factor, but did not specify hatcheries of origin.^31–33 While contact with poultry was an identified risk factor for infection for a majority of cases, data on specific behaviors related to poultry contact were typically missing.

In 2013, the largest reported Salmonella outbreak (Salmonella serotype Typhimurium) from live poultry occurred with 356 identified cases across 39 states, and 26% of the cases were hospitalized.²⁹ A single hatchery in New Mexico was identified as the supplier. Another notable recent outbreak (S. Montevideo) extended from 2004 through 2011, involving 316 cases in 43 states.²² This strain primarily affected young children (median age 5 4 years) and was linked to contact with live poultry from a single, unspecified mail-order hatchery in the western United States. The lengthy time span of this outbreak reflected challenges in identifying the source, linking cases, and reducing risk.

DISCUSSION

Given the relevance of Salmonella in human disease from contact with live poultry, understanding transmission pathways for this pathogen from poultry to people is critical. Poultry shed Salmonella in feces, and direct or indirect contact with poultry fecal material can result in exposure.³⁴ Pathogenic fecal bacteria can be found on the beak, feathers, or feet of live poultry. Egg handling and consumption also poses opportunities for pathogen transmission, as eggs may be contaminated with fecal matter, and hand hygiene following collection of eggs from backyard chickens is often insufficient.^35,36

Chicks are introduced into the household either directly from the hatchery, from a feed store, or from a local breeder. Once in the household environment, humans may be exposed to Salmonella from direct contact with live poultry (e.g., snuggling or kissing chicks, incomplete hand hygiene following poultry contact, or through slaughter).⁴ Children may be at particular risk as they are more likely to touch, kiss, or snuggle live poultry (particularly chicks), put their hands in their mouth, and inconsistently practice hand washing. Handling infected, ill, or dead poultry also poses a risk for pathogen transmission, as does animal slaughter.

Indirect exposure to poultry fecal pathogens can occur following fecal contamination of the environment.³⁷ Bacterial pathogens from poultry feces may remain infectious in environmental media from several days to months, and can contaminate soil, water, and air.^38,39 Transmission of pathogens into the home and outside the backyard may occur via shoes and clothing worn in the coop. Wild animals in the urban environment, including rodent and avian species, may have contact with poultry coops, resulting in interspecies transmission of pathogens. Likewise, domesticated animals may carry pathogens into the household from the backyard, or may become infected themselves.⁴⁰

Shaping urban poultry ordinances to reduce infectious disease risk

To reduce infectious disease risk from contact with live poultry, urban poultry ordinances should include the following components: limited flock size, safe composting of poultry fecal waste, prohibition of slaughter at the home, required veterinary care in the event of bird illness, appropriate disposal of dead birds, annual permitting linked to consumer education, and a regularly updated registry of households with live poultry (Figure 2). These guidelines reflect an understanding of pathways of Salmonella transmission from backyard poultry to humans and have two central goals: (1) to reduce human contact with infectious animal material and (2) to provide information on the scope and location of poultry within the jurisdiction for planning purposes.

Figure 2.

Guidelines for urban backyard poultry regulations to reduce the risk of zoonotic pathogen exposure

Limiting flock size.

Controlling flock size reduces (1) opportunities for pathogen transmission from other animals to poultry, (2) the risk of human infection from contact with poultry, and (3) the infectious burden of manure that could contaminate the environment. The number of animals permitted may vary depending on a typical lot size, but should be appropriate for the region.

Compost poultry manure in sealed containers.

Appropriate disposal of poultry fecal waste is imperative to reduce the risk of human infection. Owners should be required to compost poultry litter in a manner that allows for pathogen die-off, prevents animal contact with the waste, and prevents contamination of the environment with poultry manure. One such approach is to compost manure in an enclosed container (e.g., a 55-gallon barrel) along with soil and carbonaceous materials, such as leaves, for a minimum of 120 days before the manure is applied to soil as compost.²⁸

Prohibit slaughter at the home.

Slaughtering animals on site in urban environments poses opportunities for pathogen transmission from infectious birds to the environment, humans, and other animals. The urban household environment is not well suited for containment of pathogens from the slaughtering of birds, including viscera, blood, and feces, and in particular may draw wild and domesticated animals to the premises, thereby increasing the risk of pathogen transmission.

Require veterinary care in the event of illness.

Mandating veterinary care for sick animals increases the likelihood of identifying infectious agents in poultry and reduces opportunities for direct and indirect pathogen transmission to humans.

Disposal of dead birds.

Dead birds must be disposed of in a way that minimizes human exposure and pathogen contamination of the environment. Dead birds could be composted in the same manner as fecal waste, such as by combining carcasses with a carbon-bulking agent in an appropriate composting container for 120 days. Dead birds could also be disposed of in the municipal trash, depending on local regulations for biohazard disposal. Double-bagging dead animals prior to disposal in the trash would reduce the potential risk of pathogen transmission and odors. Dead animals should not be transported to municipal facilities in private vehicles for disposal, as they may contaminate vehicles.

Link permitting to consumer education on hygiene.

Issuing permits for poultry ownership and requiring permit renewal annually present important opportunities for ongoing education, communication regarding disease risk, and enforcement. Owners should be required to obtain a permit prior to poultry ownership and renew their permit on a regular basis. Education on hygiene, protective equipment, and zoonotic disease should be a requirement for receiving a permit or renewal. For example, permit applicants could be required to engage with an interactive module online and answer questions regarding disease transmission risks from poultry prior to receiving a permit. Such training could be required annually as part of the permit renewal process.

Maintain registry of households with poultry.

The jurisdiction's ordinances should require the jurisdiction to maintain a registry of households with poultry. Such data could be gathered by permitting. Understanding the spatial distribution of poultry in the city may assist in modeling disease outbreaks or planning interventions.

CONCLUSIONS

The reintegration of live poultry into the urban environment poses risks to human health due to zoonotic disease transmission from poultry to humans. Noncommercial contact with poultry has been associated with numerous multistate Salmonella outbreaks in recent years and poses risks for transmission of other bacterial and viral pathogens. The local nature of poultry regulation poses challenges for systematically managing infectious disease risk from backyard poultry, and many U.S. urban ordinances do not fully address the infectious disease risks to humans associated with this practice. Urban poultry ordinances should incorporate specifications regarding maximum flock size, manure management, slaughter and disposal, veterinary care, permitting, and consumer education and develop and maintain a registry of households with poultry to aid with public health planning. The incorporation of this framework into urban poultry ordinances will help reduce the risk of infectious disease associated with backyard poultry ownership in U.S. cities.