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A survey of selected avian pathogens of backyard poultry in northwestern Ecuador.

Abstract: As part of a larger ecologic research project and to collect disease prevalence information on backyard chicken flocks in northwestern Ecuador, 100 randomly selected birds from 10 flocks were examined, and blood, fecal, and ectoparasite samples were collected. The owners of the flocks were surveyed regarding flock management and disease history. Mean flock size was 20 birds (range, 1-75), and birds were kept for eggs and meat for either domestic consumption or local sale. Vaccination rates were low, with most owners (8 of 10) not vaccinating at all and some (2 of 10) vaccinating with one product either sporadically (1 of 10) or annually (1 of 10). None of the owners treated their chickens for parasites. Mortality rates of offspring were reported as high as 50% (range, 35%-50%) per flock. Deaths were associated with diseases described by owners as causing neurologic signs, sudden death, or respiratory problems. In addition, owners described epizootics of wartlike seasonal skin lesions, presumably but not confirmed as avian pox. Results of commercial enzyme-linked immunosorbent assays on serum samples showed that birds had antibodies against infectious bursal disease virus (100%), Newcastle disease virus (97%), avian encephalomyelitis virus (92%), chicken anemia virus (90%), infectious bronchitis virus (85%), Mycoplasma gallisepticum (73%), and Mycoplasma synoviae (68%). Although 11% of birds showed the presence of antibodies for avian influenza, antibody levels were low in all but 4 birds. Most birds (90%) had feather mite infestations. Results of necropsy and fecal examinations found low levels of internal parasitism, with cestodes and ascarids identified as the most prevalent endoparasites. Ectoparasites identified were Dermanyssus gallinae and Ornithonyssus bursa. The poultry diseases to which sampled chickens had been exposed are likely the cause of the high mortality rate reported by flock owners. In these backyard poultry flocks in Ecuador, preventive medicine protocols that provide realistic cost-benefit advantages should be implemented. Because wild birds are susceptible to some poultry diseases, free-roaming chickens might be potential vectors of pathogens that could affect wild birds.

Key words: bird conservation, Ecuador, avian, backyard chicken, poultry, disease


Infectious diseases have long been recognized as a major factor affecting the population dynamics of free-ranging species. (1) More recently, infectious diseases have been responsible for major declines of wild animal populations. (2) Therefore, conservation efforts should consider the health issues that affect wildlife. (3,4) In the past, studies of diseases in free-ranging wildlife were limited to zoonoses or to species or diseases of economic significance or were triggered by an event that caused a significant negative impact, for example the epizootic of morbilli viruses in marine mammals. (5) Disease issues affecting wildlife have been linked to a variety of anthropogenic activities, (6) such as introducing new pathogens or exotic species or modifying habitat, leading to an increase in disease prevalence or environmental contamination. (7-9) However, a new approach should be pursued that encourages the study of human effects on the health of populations, communities, or ecosystems before catastrophic events occur. (4,6,10)

Ecuador is recognized as a high priority area for biodiversity conservation. (1l-13) Within Ecuador, the Choco-Andean region shelters 4% of bird species on the planet. Given that it has the highest number of endemic bird species, this area is considered by scientists as a "global priority zone." (1l) Therefore, preserving avian biodiversity in this region should be a priority. (14) As evidenced by disease issues in the conservation of Hawaiian birds and recent emerging diseases such as West Nile virus and Mycoplasma species conjunctivitis, infectious disease can play a significant role in the dynamics of wild avian populations and should be investigated. (15-17) Unfortunately, few studies shed light on disease agents that affect neotropical wild birds. (18,19)

The project we describe is part of a larger ecologic study aimed at understanding the relationship between human-induced land use changes and the prevalence and diversity of pathogens in avian communities in 4 land use types: primary and secondary low montane forest within a private reserve, "eco-friendly" agricultural land, and active agricultural land. Although the effect of anthropogenic habitat modification on birds has received substantial attention, studies have focused on the context of population distribution, diversity, and abundance. (20-24) None of these studies included a component that investigated health or disease.

The first phase of this project involved describing selected pathogens of a variety of free-roaming backyard chickens in northwestern Ecuador (0[degrees]13'0"S, 78[degrees]63'30"W) immediately surrounding the Maquipucuna Reserve. Chickens are often used as sentinel species to monitor the presence and prevalence of certain infectious diseases and, in most cases, are considered good indicators of avian disease agents in a given environment. (25,26) In this study, chickens were used to determine the pathogens to which wild birds that exploit anthropogenic habitats might be exposed. Second, backyard flocks of chickens living in and near the village often stray into forest patches and share food and water sources with wild birds, potentially creating opportunity for disease transmission to free-ranging birds. Examples of avian species that were observed within anthropogenic habitats and either fed, roosted, or both within villages and farms include the smooth-billed ani (Crotophaga ani), common nighthawk (Chordeiles minor), white-collared swift (Streptoprocne zonaris), Pacific hornero (Furnarius cinnamomeus), lemon-rumped tanager (Ramphocelus icteronotus), swallow tanager (Tersina viridis), blue and white swallow (Notiochelidon cyanoleuca cyanoleuca), blue-black grassquit (Volatinia jacarina), shiny cowbird (Molothrus bonariensis aequatorialis), turkey vulture (Cathartes aura), black vulture (Coragyps atratus), cattle egret (Bubulcus ibis), and a variety of members of the Tyrannidae family (flycatchers) and Troglodytidae (wrens). Birds that utilize forest into which chickens roam and that have ecologic behaviors that might put them at risk of coming into contact with poultry and poultry feces include ground birds (or those that spend a significant amount of time on the ground), such as Tynamidae (tinamous), Columbidae (pigeons and doves), Thamnophilidae (antbirds, antshrikes), Caprimulgidae (nightjars and nighthawks), Furnariidae (foliage gleaners and leaf tossers), Formicaridae (antpittas), Emberizidae (finches and grassquits), or Turdidae (thrushes), and birds that might either consume chickens or aggregate near foodstuff consumed by chickens, such as Cathartidae (vultures), some members of Accipitridae and Falconidae (hawks, eagles, falcons), Cracidae (guans), and Odontophoridae (quails). This list is not complete because birds that do not spend time on the ground, but roost, nest, or feed in trees where chickens are roosting, might also be considered. Lastly, eco-friendly agricultural land, such as shade-grown coffee plantations, is promoted in this region as a way to enhance biodiversity because it provides more suitable habitat and supplemental food (ie, banana) for forest birds than pasture, monoculture crops, or other types of traditional agriculture. However, shade-grown coffee plantations are managed much like traditional agricultural land, which often translates to domestic animals having access to these "forests," creating an additional source of contact between chickens and forest birds.

Several investigations have supported the theory that wild birds play a small role in domestic bird disease. (27-31) However, research into the details of disease transmission from free-roaming backyard chickens to wild birds is scant. (32-34) The negative effect of backyard chickens on human health, especially as it relates to children, has been reported and is of concern, especially in developing nations. (35-39)

Poultry production is a growing industry in Ecuador. Two new commercial and several small-scale poultry operations have been developed in the vicinity of the Maquipucuna Reserve. The poor husbandry practices often used in backyard flocks make these flocks a potential reservoir for diseases that can affect commercial poultry operations, especially diseases that have become rare in these operations. (40,41) Investigations that effectively link human, animal, and ecosystem health are rare but should be supported. The objective of this study was to investigate the diseases of free-roaming chickens in northwestern Ecuador and is presented here as the preliminary phase of a larger effort in multidisciplinary conservation medicine.

Materials and Methods

Owner surveys and animal examinations

Ninety-nine chickens (Gallus domesticus) and one turkey (Meleagris gallopavo gallopavo) that belonged to 10 private individuals were randomly captured for examination and blood collection during a 10-day period in December 2003. Twenty-three animals belonged to an organic farm managed by the Maquipucuna Foundation and were kept in a fenced yard. The rest were free-roaming domestic birds living in the town of Santa Marianita, Ecuador, or in farms on the outskirts of the town. The town of Santa Marianita is located in the Pichincha province in the northwestern portion of Ecuador, 4 km outside of the southwestern edge of the Maquipucuna Reserve at 1300 m elevation. It is the last town in which tourists can stop before entering the Maquipucuna Reserve and Ecolodge. The population of Santa Marianita is approximately 225 members, with most families living in a central area dedicated to residences and others living in surrounding farms. The landscape surrounding the village is composed of active agricultural land (pasture, sugar cane, and fruit trees) or low montane forest in varying stages of regeneration. All birds sampled were numbered sequentially from 1 to 100. Of the chickens sampled in this study, 45 came from dwellings in the center of village (approximately 20 dwellings in a semicircle surrounding a soccer field; Fig 1). The remaining chickens sampled came from flocks in surrounding farms (Fig 2). All of the farms were within a 2-km radius of the village proper. The local chicken breed is a "creole" native red chicken, although 1 chicken examined was a silkie and 5 were Transylvanian naked necks.


All chickens were examined before samples were collected. A physical examination was performed to gauge body condition by palpating the pectoral musculature (scored from 1 to 5 of 5, where 1 = emaciated, 2 = thin, 3 = ideal, 4 = overweight, and 5 = obese), to subjectively assess the presence and degree of mite infestation (scored as low = <50 mites/1 wing, moderate = 50-150 mites/wing, or severe = >200 mites/wing), and to detect any notable abnormalities. The same researcher scored all animals in this study to avoid sampling bias. Birds with a body condition of 3/5 or less or with severe mite infestation or other physical abnormalities were considered abnormal. The number of abnormal birds per flock was recorded. Ectoparasites were collected and immersed in 70% ethanol for later identification by a parasitologist on the basis of morphologic characteristics. Approximate age of each bird was estimated on the basis of spur length and information provided by the owner according to the following scale: spur length <1.3 cm (1/2 in), juvenile bird; spur length 1.3 to 2.5 cm (1/2-7/8 in), 1-year-old bird; and spur length [greater than or equal to] 2.5 cm (7/8 in), 2-year-old or older bird. Approximate age, breed, and sex were recorded for each bird.

All owners were interviewed during the sampling procedure by the primary author. Standardized survey questions were source of chickens; total number of chickens; purpose for maintaining chickens; age at time of slaughter or sale; whether chickens were penned at any time; approximate mortality rate; description of the clinical signs perceived as associated with disease; perceived needs for improving production, vaccination history, and nutrition; and medication history of chickens. Although all chickens appeared to roam freely throughout the village and surrounding areas, each owner claimed they could recognize their own animals.

Sample collections

Blood samples (3 ml) were collected from each of the 99 chickens and 1 turkey from either the right jugular vein or the superficial ulnar vein. One blood smear was made immediately, and the remaining blood was placed in a sterile clot tube. The blood smears were dried, stained with Wright stain, and stored. The blood samples were maintained in a cooler with ice and centrifuged no more than 8 hours after collection. After centrifugation, approximately 1.5 ml of serum was transferred to cryovials and frozen at -18[degrees]C. Blood products were prepared for importation following United States Department of Agriculture (USDA) guidelines for pathogen inactivation.

At least 5 fresh fecal samples were collected from each flock. Fifty fecal samples were examined for parasites by direct smear and fecal flotation on the day of collection, then discarded. Standard flotation techniques with sodium nitrate and Sheather sugar solutions followed.

Blood smears were examined for the presence or absence of hemoparasites by examining the entire blood smear at x 100 magnification to detect microfilaria then examining the monocellular layer at x400. To determine disease seroprevalence, commercial enzyme-linked immunosorbent assays (ELISAs; Idexx Inc, West Brook, ME, USA) were performed for infectious bursal disease (IBD, gumboro disease), avian encephalomyelitis virus (AE, Picornaviridae), chicken anemia virus (CAV, Circoviridae), Newcastle disease virus (NDV, Paramyxoviridae), avian influenza (Orthomyxoviridae, type A), avian infectious bronchitis (IBV, coronavirus), Mycoplasma gallisepticum, and Mycoplasma synoviae (University of Georgia Poultry Diagnostic and Research Center, Athens, GA, USA).

Sample-to-positive (S/P) ratios were calculated from absorbance values by the formula

S/P ratio

= [Sample mean - negative control mean]/[Positive control mean - negative control mean].

The S/P ratio is then converted to the antibody titer by a computer program developed by the manufacturer. Results were considered positive if the S/P ratio was >0.2 for Newcastle disease virus, infectious bursal disease, infectious bronchitis virus, and avian encephalomyelitis virus or >0.5 for M gallisepticum, M synoviae, and avian influenza. For chicken anemia virus, results were considered positive when the optical density was <1.08. Capture ELISA to detect immunoglobulin (Ig)M and IgG against West Nile virus was performed at the University of Georgia Veterinary Diagnostic Laboratory (Tifton, GA, USA).

Necropsy examinations

Ten chickens that belonged to 3 different owners and that were not part of the previously sampled group were examined and humanely euthanatized. Necropsy was performed immediately after euthanasia. For each bird, a representative sample of organs (skin, muscle, nerve, trachea, thyroid, thymus, lung, air sac, heart, liver, spleen, kidney, adrenal, gonad and accessory structures, eye, brain, pancreas, esophagus, proventriculus, ventriculus, small and large intestine, cloaca, and bone) were collected and preserved in 10% buffered formalin for importation according to USDA Guidelines for pathogen inactivation. Parasites were collected into 70% ethanol for transport and subsequent identification. Blood smears, parasites, and tissue and serum samples were imported into the United States under a zoosanitary certificate, issued by the Ministry of Agriculture and Livestock of Ecuador (#051643), and a USDA permit for importation of controlled materials, organisms, and vectors (#46302 and #27556).


Owner surveys and animal examinations

Private individuals maintained chickens primarily for eggs, personal use of the meat, breeding, and cockfighting. Mean flock size was 20 birds (range, 1-75). None of the chickens examined in this study were cockfighting roosters; however, these roosters often foraged or were housed in contact with the free-roaming chickens. In general, owners reported that they bred their own chickens and kept most of the offspring; however, in some instances, owners mentioned that they traded or sold chickens with nearby villages. Chickens were slaughtered at 36 months or sold at 24 months. Fighting cocks were often traded or sold. None of the owners maintained formal records; however, all recognized which animals belonged to them. The area where their chickens foraged was reported to be between 200 and 300 m away from their respective homes. Owners captured and penned hens only when they were broody and thus incubating fertile eggs. Otherwise, except for fighting cocks, which were penned some of the time, chickens were not provided with permanent housing. Birds roosted in trees or on building structures at night. The chickens primarily foraged for food in active agricultural land and surrounding forest but were also supplemented daily with corn and, rarely, commercial poultry rations. Only fighting cocks were fed poultry rations regularly.

The disease syndromes that were perceived as the most important and that caused mortality in the flocks were 1) mal de pollo (chicken plague), described as an acute disease during which most chickens in the area died suddenly or exhibited neurologic signs and which owners perceived as contagious and capable of spreading from flock to flock; 2) skin lesions, described as wartlike lesions on the head, face, and legs of the birds that were most prevalent during the dry season but caused little mortality; 3) ronquera (rales), a respiratory syndrome in which chickens exhibited mucopurulent discharge from the nares, excessive tearing, gasping, loud respiratory sounds, weight loss, and in some cases, death; and 4) a syndrome in which chickens became pale, lost weight, and died. Owners reported an overall annual mortality rate of between 35% and 50%. A 50% mortality rate was reported in chicks in the first 4 weeks of life, with diarrhea and respiratory signs cited as the top 2 reasons for death. Most owners (8 of 10) reported that they did not vaccinate at all. One owner reported vaccinating chickens when an outbreak of real de pollo was occurring in the village; however, the specific vaccine used was not known. A second owner vaccinated annually with the same product. Although the particular product was not available for inspection at the time of this study, the local supplier was questioned and confirmed that Newcastle disease vaccine was sold to village owners. None of the owners treated their chickens for ecto- or endoparasites.

The percentage of abnormal physical findings in the chickens from each flock varied from 4% to 25%. The owner with the largest flock (75 chickens) had the lowest number of abnormal animals. Abnormalities found were: moderate to heavy mite infestations (14%); thin body condition (10%); rhinitis (5%); poor feather condition (5%); evidence of previous pox lesions on head, face, or legs (4%); increased respiratory effort (3%); and conjunctivitis (1%).

Serologic test results

In 21 (21%) birds, antibody levels were above the seropositive threshold for avian influenza. Of these, 1 (S/P ratio 5.209) was likely caused by system error because of a dirty sampling cell (possibly from bacterial growth). In 6 samples, the S/P ratios were slightly greater than 0.500 (0.526-0.575). In 10 samples, the S/P ratios were higher (0.6340.993); however, all of these results were lower than those in birds infected with avian influenza. In 4 samples, results were typical of birds infected with avian influenza (1.081-1.756). Therefore, 16 of the 21 samples had low S/P ratios and were considered negative.

Of the 100 birds tested for antibodies, 100 (100%) were positive for infectious bursal disease, 85 (85%) for infectious bronchitis virus, and 97 (97%) demonstrated antibodies for Newcastle disease virus. Ninety-two (92%) showed antibodies (titer >1500) for avian encephalomyelitis, with no difference in seroprevalence among flocks. In 90 (90%) birds, antibodies were detected for chicken anemia virus. Seventy-three (73%) had antibodies against M gallisepticum, whereas 68 (68%) had antibodies against M synoviae. Antibodies against M gallisepticum or M synoviae were not present in one of the flocks tested. A histogram summarizing titer levels of each disease for all animals is presented in Figure 3.



No hemoparasites were found in the 100 blood smears examined. Parasites collected at necropsy were identified as cestodes (Raillietina species) and ascarids (Ascaridia species). Two species of ectoparasites were collected and identified as Dermanyssus gallinae and Ornithonyssus bursa. On direct examination of fecal samples, 2 samples were positive for parasites: 1 contained strongyle-like eggs and the other contained coccidian-like cysts.

Necropsy and histopathologic results

Of the 10 birds submitted for necropsy, 9 were in fair to good body condition. Tapeworms were present in the upper and middle third of the small intestine in 8 birds. One bird exhibited hemorrhagic enteritis, and 1 bird had splenomegaly. In 2 birds, the liver had pale streaks throughout the parenchyma. One animal was extremely thin and had wartlike lesions on its head, severely thickened air sacs, a consolidated right lung, and a large number of tapeworms and ascarids.

All 10 chickens had mild, nonspecific infiltrates of few lymphocytes and plasma cells in various organs, such as liver, kidneys, heart, and lungs. These infiltrates were very minimal, similar to those seen in commercial poultry, and not indicative of any particular disease. Specific lesions observed in all chickens were marked infiltrates of lymphocytes and plasma cells in the mucosa of the small and large intestine, sometimes accompanied by loss of crypts in both small and large intestine and mild atrophy of villi in the small intestine. Germinal centers were also occasionally seen in small and large intestine. Numerous sarcomastigophoran protozoa were present in the large intestinal crypts in 7 birds. These protozoa appeared amoeboid, were 10 to 25 [micro]m in diameter, and were confined to the crypt lumen. Morphologically, protozoa were most consistent with an amoeboid Entamoeba-like organism.

Other parasites were found in several birds. Histologic evidence of nematode infection was found in the proventriculus, ventriculus, small intestine, or cecum in 4 chickens. Inflammation in the wall of the ventriculus in 1 bird was consistent with previous parasite migration. Cestodes were also confirmed histologically in the intestinal lumen of 2 chickens. One chicken had numerous sarcocysts in its skeletal muscle, 1 had respiratory mites identified histologically, and 1 had evidence of pulmonary inflammation with mite debris in its lungs.

One chicken had an enlarged spleen from the presence of numerous adenoviral inclusions in the nuclei of splenic macrophages. These inclusions were large and lightly basophilic and compressed the chromatin to the periphery of the nucleus. These inclusions were consistent with infection with a group II avian adenovirus, such as the viruses that cause hemorrhagic enteritis in turkeys, marble spleen disease of pheasants, and adenovirus-associated splenomegaly in chickens. Although these viral infections can cause serious disease, particularly in young birds, this chicken appeared relatively healthy and was reproductively active. Histopathologic examination of the wartlike skin lesions revealed proliferative epithelial cells exhibiting ballooning degeneration with eosinophilic intracytoplasmic inclusion bodies, confirming a diagnosis of avian pox. Another chicken had severe, chronic bacterial pneumonia from a small bacterial rod, most consistent with an enteric organism such as Escherichia coli or possibly Pasteurella multocida. Histologic evidence of a preexisting lower respiratory tract disease was not present in this chicken; therefore, the infection was likely primary, and not secondary, to another infection such as Newcastle disease or mycoplasmosis. Other than the 2 isolated findings of adenoviral splenitis and bacterial pneumonia and evidence of parasitism, avian pox, and chronic enterocolitis, no other significant disease was evident histologically in this group of 10 chickens.


In this study, backyard poultry in Ecuador showed evidence of exposure to important poultry pathogens. These disease pathogens, both singly and in combination, are likely responsible for the high mortality of young birds and potentially for decreased reproductive success of adults. Possibly, chickens from other towns that are sporadically purchased or introduced into backyard flocks act as disease reservoirs, and this practice might relate to the epizootics reported by owners. In general, production in these free-roaming flocks is poor. The overall high mortality rate reported by owners indicates that the chickens would benefit from a detailed preventative medicine protocol. Peer-reviewed sources that outline protocols for backyard flocks, especially those that consider cost: benefit ratios for the owners, are rare. (41) Given the potential hazard to human and wildlife health, as well as threats to commercial operations, a thorough review of backyard flock preventative medicine is long overdue.

Preventative medicine in chickens has been proved to decrease production loss and mortality. (42) However, lack of education and cost of preventative measures preclude the owners in this village in Ecuador from applying standard preventative medicine protocols, increasing the susceptibility of the chickens in their flocks to a variety of bacterial, viral, and parasitic diseases. The high mortality rates reported are directly linked to the lack of preventative medicine and shelter, the practice of keeping chickens of different ages in the same group, and allowing new chickens to be introduced into existing flocks in the village.

The liquid vaccine used by 2 owners was likely a vaccine prepared for Newcastle disease, as this is the most commonly administered vaccine for poultry available in Ecuador. However, it was inappropriately stored and administered and thus unlikely to have been effective. Five months after this project was completed, another outbreak caused sudden deaths in more than 30 chickens after chickens from Quito were introduced. The owners described it as real de pollo. Because our survey did not take place during an outbreak, we did not perform diagnostic tests to investigate the cause. However, considering the history and clinical signs, the high prevalence of Newcastle antibodies among this population of chickens, the high antibody titers against Newcastle disease virus, and results of consultation with government veterinarians and poultry veterinarians with experience in Ecuador, we concluded that this plague was most consistent with an outbreak of Newcastle disease. Indeed, in the older literature, Newcastle disease is referred to as chicken plague, and in some Spanish-speaking countries, Newcastle disease is often termed plague.

Although avian pox was confirmed only in 1 chicken, our survey was conducted during the rainy season, a time when owners reported the lowest prevalence of wartlike lesions. We are confident that avian pox is a likely diagnosis for the aforementioned skin lesions. Given the results of serologic tests and questionnaires, the respiratory disease described by owners likely was caused by either Newcastle disease virus or infectious bronchitis virus. It is more difficult to speculate on the last of the 4 major diseases causing significant mortalities in these flocks, described as causing anemia, weight loss, and death. Tumors caused by Marek's disease or leucosis might explain these clinical signs.

Most chickens would be expected to have been exposed to avian encephalomyelitis, infectious bursal disease, infectious bronchitis virus, chicken anemia virus, Newcastle disease, and M gallisepticum/ M synoviae. The USDA lists Ecuador as a country with endemic exotic Newcastle disease, as well as the other typical poultry diseases. (43) The positive titers on ELISA tests indicate that these chickens were exposed to these diseases at some point and survived the infection. None of the birds examined exhibited clinical signs consistent with these diseases; therefore, no definitive comment can be made about whether the chickens expressed clinical disease after exposure. However, usually an antibody titer can only result from exposure to those particular pathogens and not from maternal antibodies or previous vaccination, particularly for Newcastle disease, infectious bursal disease, infectious bronchitis, and Mycoplasma species.

Given the significance of avian influenza, the results obtained in this study were carefully examined. The threshold for a seropositive result for the ELISA, as determined by the manufacturer, is 0.500 S/P. Of the 21 positive samples, 1 was likely laboratory error. In 6 samples, S/P ratios were slightly above the threshold value and unlikely to be true positives. In 10 additional samples, S/P ratios were not as high as those usually seen in birds infected with avian influenza. Therefore, only 4 samples had results typical of birds infected with this disease. However, given the highly transmissible nature of avian influenza, it is unlikely that 4 birds would be infected without the rest of the flock also exhibiting seroprevalence. Current reports of avian influenza outbreaks demonstrate seropositive rates greater than 90% in infected flocks. To further confirm the presence of antibodies for avian influenza in the seropositive birds, agar gel immunodiffusion (AGID) testing could be done; however, this was not done in our study because of insufficient amount of serum.

Only one significant difference was seen in disease seroprevalence among flocks. One flock, located 2 km from the village, showed no seroprevalence to M gallisepticum or M synoviae. The chickens in this flock were not in contact with chickens from other farms or villages. Indeed, even in commercial operations, the seroprevalence of Mycoplasma can vary, with some flocks having 0% seroprevalence. (43) Seroprevalence rates for the remaining diseases did not differ among flocks, indicating that those birds kept in more isolated farms were exposed to the same diseases as birds kept within the village proper.

Free-roaming chickens are commonly exposed to a variety of parasitic diseases. In young birds, heavy infections of cestodes can result in reduced efficiency and slower growth. (43) Poultry become infected by ingesting the intermediate hosts of cestodes such as snails, slugs, beetles, ants, grasshoppers, earthworms, houseflies, and other arthropods. The intermediate host becomes infected by eating the eggs of tapeworms that are passed in the bird feces. The host of Raillietina species is a beetle, and foraging chickens have ample opportunity to ingest this and other arthropods. Ascaridia species, the largest internal nematodes that infest the small intestine, can cause poor body condition and intestinal impaction. Heavy infestations can cause death. Chickens 3 to 4 months of age show resistance to infection. (43) The worm is transmitted vertically from hen to offspring; therefore, infected adults can be source for young. (43) Additionally, embryonated ascarid eggs are very hardy and, under laboratory conditions, can survive for 2 years. However, in field conditions, few probably survive more than 1 year. (43) Chickens become infected by ingesting eggs that have reached the infective stage. At necropsy, most chickens that were examined had either no or low numbers of ascarids in the intestines. One chicken that had a heavy load of ascarids also had severe pneumonia. Fecal flotation examination yielded a very small number of parasites per sample and in total.

In general, intestinal parasitism was not a major concern in this group of chickens. This was expected because, as opposed to commercial poultry operations, chickens in free-roaming conditions are not concentrated in small areas, do not frequently come in contact with the fecal material of other chickens, and are not confined to contaminated bedding. Parasites that require an intermediate vector were observed in these birds but were not of major concern. It is difficult to ascertain how the ectoparasite infestations observed in these birds affected their health. In commercial operations, ectoparasites can affect production, but because production is not monitored in these flocks, it could not be correlated with levels of ectoparasites.

On histopathologic examination, the marked infiltrates of lymphocytes and plasma cells identified in the mucosa of the small and large intestine indicate that these chickens probably survived an episode of enterocolitis, resulting in the residual inflammation. A specific cause was not observed in any chicken. The amoeboid protozoa found in the intestine, morphologically consistent with Entamoebae, have been described previously parasitizing the intestinal tract of chickens, but their significance is uncertain. (43) Because amoeboid protozoa were present in only 7 birds, they are not likely to be the only cause for the prominent intestinal inflammation in all birds. The chronic enterocolitis could indicate previous exposure to other intestinal pathogens, such as Salmonella; however, this was not confirmed. Further investigation into the bacterial pathogens, including microbiologic culture of fecal samples of these chickens, is warranted.

Compared with commercial poultry, free-roaming chickens are both at an advantage and disadvantage for maintaining health. Free-roaming chickens do not receive vaccinations typically given to commercial poultry, including vaccinating hens to increase maternal antibody transferred to chicks. This renders free-roaming chickens inherently more susceptible to many infectious diseases. Additionally, free-roaming chickens are not given treatments commonly used in commercial poultry, such as coccidiostats. Free-roaming chickens are unlikely to be on the same nutritional plane as commercial birds, which are provided a complete, balanced, pelleted diet. Commercial birds are maintained in single age groups in an "all in, all out" manner, whereas free-roaming chickens are in flocks of mixed ages, with susceptible young chicks in contact with adults that are potential reservoirs of disease. Therefore, an infectious disease could easily be maintained in a free-ranging flock by a continuous supply of new susceptible hosts coming into contact with reservoir animals. Last, most commercial poultry breeder flocks are maintained free of certain infectious diseases that can be transmitted from the hen to her progeny, including Salmonella pullorum, Salmonella gallinarum, M gallisepticum, and M synoviae. Because free-roaming chicken flocks are not monitored for these diseases, diseases could remain endemic in the population through continued egg transmission.

Free-roaming chickens have the advantage of not being reared or maintained in confinement at the intense stocking densities that are typical of commercial poultry. In some commercial poultry operations, birds are commonly reared and maintained on used litter that potentially harbors pathogens. Certain diseases in commercial birds, such as coccidiosis and Marek's disease, are perpetuated by these management practices. (43) These diseases would be expected to have little effect on free-ranging chickens because they are not exposed to contaminated litter and dander in a confinement situation.

The diseases for which these birds were tested have significant economic importance in the poultry industry. (43) Commercial poultry is a rising industry in Ecuador. Two commercial poultry operations are located near the town of Santa Marianita, and although biosecurity is stringent in these operations, it is important for the Ecuadorian authorities to be aware of the diseases harbored by free-roaming chickens, in case of a biosecurity breach that might lead to an epizootic.

In this study, the only zoonotic disease agent detected was Newcastle disease virus, which can cause photophobia and transient conjunctivitis in people. (43) However, the bacterial diseases of this group and similar flocks of chickens should be investigated because bacterial agents such as Salmonella species and Campylobacter species are more important zoonotic diseases. Additionally, salmonellosis has been implicated as an emergent disease of wild birds. (44)

The susceptibility of wild birds to poultry diseases is unknown. Several reports of Newcastle disease and highly pathogenic avian influenza infecting wild birds have been made. (12,45-48) Pathogen pollution is a term applied to the anthropogenic introduction of pathogens into new areas. (6) It is impossible to know whether these avian viruses and parasites were present in the area before the town was settled and domestic birds were introduced or whether they present a significant threat to the native avian populations. At this time, no deaths have been observed in the wild bird populations of the area; however, it is often difficult to discover dead wild birds in a remote tropical forest unless hundreds or even thousands have died. Therefore, investigating the risks that free-roaming birds and their endemic pathogens pose to wild birds would be prudent.

Acknowledgments: We thank the Maquipucuna Foundation for logistical support of this project and the following sponsors for providing financial support: Neurocare Consultants, Palm Beach, FL; Bankers Equity, Centurion Poultry, HOPE Animal Medical Center, and Jittery Joe's, Athens, GA; and Sigma Xi Grants-In-Training. We would particularly like to acknowledge the poultry owners and the Santa Marianita community. Without their trust and enthusiasm, this project could not have been realized. We also thank Dr Bolivar Valenci, who provided us with logistical support in Ecuador. Harmony Seahorn (Poultry Diagnostic Research Center, University of Georgia, Athens) provided instrumental technical assistance. We are grateful to Dr Sarah Schweitzer and Alison Lipman for review of this manuscript.


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From the Institute of Ecology (S. M. Hernandez-Divers, Carroll), the Poultry Diagnostic and Research Center (Villegas), and the Department of Pathology, College of Veterinary Medicine (Stedman), University of Georgia, Athens, GA 30602, USA; The Maquipucuna Foundation, Baquerizo #238, PO Box 17-12-167, Quito, Ecuador (Prieto, Unda); and the Exotic Animal, Wildlife, and Zoological Medicine, Department of Small Animal Medicine & Surgery, College of Veterinary Medicine (Ritchie, S. J. Hernandez-Divers), University of Georgia, Athens, GA 30602, USA.
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Article Details
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Title Annotation:Original Studies
Author:Hernandez-Divers, Sonia M.; Villegas, Pedro; Prieto, Francisco; Unda, Juan Carlos; Stedman, Nancy; R
Publication:Journal of Avian Medicine and Surgery
Geographic Code:3ECUD
Date:Sep 1, 2006
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