A DIAGNOSTIC SURVEY OF GASTROENTERIC HELMINTHS IN BACKYARD POULTRY OF A RURAL VILLAGE IN MEXICAN TROPICS

A DIAGNOSTIC SURVEY OF GASTROENTERIC HELMINTHS IN BACKYARD POULTRY OF A RURAL VILLAGE IN MEXICAN TROPICS Karen Cervantes-Rivera, José Alfredo Villagómez-Cortés, Alfredo Arroyo-Lara and Luis Antonio Landín-Grandvallet Faculty of Veterinary Medicine and Animal Science, University of Veracruz, Veracruz, Mexico E-Mail: avillagomez@uv.mx ABSTRACT A cross-sectional study was conducted to determine the frequency of gastroenteric helminths in backyard poultry in a rural village located in the hot humid tropics of Mexico. Faecal samples of 199 female and 71 male birds (43 chicks, 57 growers, and 170 adults)were examined using the modified McMaster technique. Out of the 270 birds examined, 169 (62.6%) were shedding nematode eggs. All 14 examined chicken backyards had parasitized animals. The nematode eggs encountered were those of Ascaridiagalli (62.7%), Capillariasp. (46.5%), Heterakis sp. (30.2%) and Trichostrongylus tenuis (19.5%). Out of the positives, 71 cases (42%) were mixed parasitism and 98 cases (58%) were monoparasitism. A 66.3% of female birds and 52.1% of males were positive to helminth infections. The highest frequency of helminth infections was recorded in adults (68.8%), followed by growers (56.1%) and chicks (46.5%). Overall average of eggs per gram (epg) of feces was 147±319. Female birds recorded a higher mean epg (164±359) compared to males (99±146). This study indicates that helminths are highly present in chicken in the study area with moderate to high levels of infections. It is recommended to place integrated control strategies to improve chicken productivity and enhance smallholder livelihood in these areas. Keywords: chicken, cross-sectional study, gender empowerment, parasites, poultry systems INTRODUCTION Backyard or family poultry production is an old system based on small flocks. The birds are mostly of a local,native or indigenous type, and roam the farms or village freely scavenging and searching for feed. Occasionally, they are provided with home-grown grains and minimum shelter [1]. Finzi (2000) considers that the most common and significant feature of backyard poultry is the low-input, low-output production system which is based almost entirely on native birds and local breeds [2]. These systems may seem primitive but they can be economically efficient because, although the output from the individual birds is low, the inputs are even lower or virtually nonexistent. Chickens raised under this system are generally utilized for home consumption and, when necessary, as source of additional income. Backyard poultry system is appropriate for the rural areas since it makes relatively good use of locally available resources. The requirement now is to improve these production systems in order to make the best possible use of these resources [3]. Some features of the system may hamper its productivity. Outdoor production of poultry poses a higher risk to parasitic infection, which combined with a nutritional imbalance due to an insufficient or unbalanced feeding may lead to a higher susceptibility to parasite infection. Endoparasitism has been signaled as an important factor associated with poor production of backyard chickens, since parasites compete with the birds for nutrients; some suck blood causing anaemia, while others cause anorexia and even death[4]. Despite its social importance, in Mexico and elsewhere, backyard poultry production as a productive activity has received little attention and research and related publications are scarce. No previous studies have been carried out to document the gastroenteric helminths of poultry in the hot humid tropics of Mexico. Hence, the objective of this study was to estimate the frequency and to determine the species of gastrointestinalnematodes present in backyard poultry in the Tembladeras Vista Hermosa village, in the municipality of Acatlán deperez Figueroa, Oaxaca, Mexico. MATERIAL AND METHODS Study area The research was conducted in Tembladeras Vista Hermosa village, in the municipality of Acatlán deperez Figueroa, Oaxaca, Mexico. The municipality has a total area of 790.8 km²and the main town lies at 96º36' West longitude, 18º32' North latitude and at 120 m altitude. The study village has less than 400 inhabitants. The climate is hot and humid with an average annual temperature of 25 Candan annual average rainfall of2,680mm. Rainy season usually occurs from June to October. Agriculture is the main economic occupation in the area. Sugarcane, maize, rice, coffee and various fruits are grown and dual-purpose cattle is kept. Study design The study was cross-sectional. Fourteen individual farmers in Tembladeras Vista Hermosa village were selected and interviewed using a structured questionnaire. Selection of farmers was purposive where each farmer owned chicken reared under free-range system. Sampling was based on the availability of freeranging poultry population in the village areas and the 463

willingness of farmers to be interviewed and to allow for collecting fecal samples from their birds.field study was conducted between August and October, 2015. The birds were categorized into three age groups, namely: chicks (aged < 2 months), growers (pullet or cockerel, 2 to 8 months) and adults (cock or hen, aged > 8 months) according to Magwisha et al. (2002) [5]. The ages were determined subjectively based on the size of crown, length of spur and flexibility of the xiphoid cartilage together with information provided by the poultry farmers. Faecal collection and examination for parasites Small pieces of plastic were placed on hangers or birds nightly resting sites to collect fresh fecesin the morning. Each bird was tied by a leg and confined to a particular spot. For transport to the laboratory the samples were kept in a cooler with ice. Fecal flotation methods were used for detection of parasitic infections. Parasite eggs were identified according to their morphological characteristicsusing the keys and features described by Foreyt (2002) and Zajac and Conboy (2012) [6,7].The number of nematode eggs in the faeces was quantifyed by the modified McMaster Method [8]. The type of helminths eggs and the number of eggs per gramme of faeces (e.p.g.) were recorded. The presence of coccidian oocyts was noted but quantification was not done. Data collection and analysis The following type of data was collected, flock size, sex and age group of poultry, phenotypic appearance, diet and feeding, type of housing and shelter, drinkers and feeders, presence of litter and trash, types of drugs/herbs used to deworm birds, frequency of deworming, and vaccination practices. Data was entered into a Microsoft Excel spreadsheet, analyzed by descriptive statistics and presented as tables.the frequency of parasites was defined as the total number of birds infested with a particular parasite group/species divided by the number of chicken examined at a point in time [9]. The EPG was described in terms of mean, minimum, maximum and standard deviation.the chi-square test (χ2) was used to compare frequencies among groups declaring significance at the 0.05 level. RESULTS AND DISCUSSIONS Management of poultry Poultry in this study is native to the community. Poultry is the most kept livestock and almost every household in village has about 5-50 indigenous chicken reared under free-range management system. There is about one cock per every five hens. Their breed and productive and reproductive parameters are unknown. In phenotypic terms, there are birds with curly or smooth plumage, bared neck, and with and without feathers in the legs. Feathers werebarred, black, white, red, gray and combination of colors. In this production system, the majority of interviewees keep the birds under free-range system (93%), because they own a relatively big space where animals can roam and find food by themselves, as are several species of insects, earthworms, maggots or fodder. Sometimes food is also offered as grains (mainly corn and rice), kitchen waste, and even commercial food (Table- 1).The sanitary conditions in the backyards of the community are rather inadequate, since most poultry holders lack information or knowledge necessary for optimal health and production. Animals do not have feeders and drinking fountains, so they eat their food directly from the ground and drink water from ponds or from devises containing water located in the backyard. In many cases, birds lack facilities forover night accommodation, sleeping at places like branches of trees, fences or at an yelevated place. Table-1. Management of backyard poultry in Tembladeras Vista Hermosa, Oaxaca, Mexico. Features % Raised in freedom 93 Provision of hangers 57 Night shelters have roof 50 Presence of pools and puddles 43 Drinkers provided 36 Feeders provided 14 Presence of litter and trash 14 Birds de wormed 7 Diet and Feeding Grains 100 Forage 100 Worms and insects 100 Food scraps 36 Commercial feed 14 Helminth parasites Four helminth parasite species were found, namely Ascaridiagalli, Capillaria sp., Heterakis sp., and Trichostrongylus tenuis. According to Pattison et al. (2008), A. galli, Capillaria sp. and Heterakis sp. can be easily distinguishedby their differences in macroscopicsize. A gallicauses a disease characterized by a chronic course with enteritis, obstruction and distension of bowel walls, low production, delayed in development, andsometimes death, especially in parasitized young animals. Clinical signs ofits presence include anorexia, ruffled feathers, diarrhea and emaciation[10].capillaria species include C. annulata and C. contorta in crop and esophagus and C. obstignatain small intestine[11]. The disease usually has achronic course and affects birds older than a monthold. When a large amount of these helminthes is present, its effect can be very pathogenic. Clinical signs often showed are anorexia, weight loss, ruffled feathers, diarrhea, pale comb and wattles. Most common injuries 464

are inflammation and presence offibrin in the gastrointestinal mucosa [10]. H. gallinarumis commonly found in the cecum. The clinical signs include depression, low production, diarrhea and weight loss,and the most common injury istyphlitis[7]. Trichostrongylustenuis can cause diarrhea and emaciation; droppings become liquid and stained with blood and injuries include typhlitis, colitis and small petechiae in the caecum [12]. Helminth parasites frequency Out of 270 samples taken, 169 (62.6%) were positive.out of the positives, 71 cases (42%) were mixed parasitism and 98 cases (58%) were of monoparasitism. Only in three subjects, the presence of the four identified helminthes was found (Ascaridiagalli, Heterakis sp.,capillaria sp., and Trichostrongylus tenuis); in 29 subjects there were three helminthes involved (Ascaridiagalli, Heterakis sp., Capillaria sp., 13; Ascaridiagalli, Heterakis sp., Trichostrongylus tenuis, 7; Ascaridiagalli, Capillaria sp., Trichostrongylus tenuis, 5; Ascaridiagalli, Heterakis sp., Trichostrongylus tenuis, 2; Heterakis sp., Capillaria sp., Trichostrongylus tenuis, 2). The most frequent parasitism by two species occurred by Ascaridiagalli and Capillaria sp. (19) and by Ascaridiagalli and Heterakis sp. (19),and in decreasing order Heterakis sp. and Capillaria sp. (7), Capillaria sp. and Trichostrongylus tenuis(2) and Heterakis sp. and Trichostrongylus tenuis (2). Parasitism by Ascaridiagalli was observed in most cases (48), followed by Capillaria sp.(27), Heterakis sp. (13), and10 Capillaria sp.(10). In Phiriet al. (2007) study in Zambia Central mixed infections accounted for 88.2% as compared to 7.2% of single infections. In the current study, Ascaridiagalli was the most frequently observed egg (62.7%), followed by Capillariasp. (46.5%), Heterakis sp. (30.2%), and Trichostrongylus tenuis(19.5%)[13]. Even though the frequency is higher, the species found are similar to those reported in Yucatan, Mexico, Ascaridia sp. (15.2%), Heterakissp. (15.3%), and Capillariasp, (6.6%)[14]. Andy-Chimbo (2014) found a prevalence of 46% in backyard poultry in Ecuador, finding Capillaria spp (58.9%), Strongyloides sp. (23.9%) and Heterakis gallinarum (14.2%)[15].Phiriet al.(2007) found a parasitism rate of 95.2% in free-range chickens of Central Zambia, a much higher frequency than the one reported in this study; they found A. galli (28.8%) and H. gallinarum (32.8%), but also higher frequencies of Allodapasuctoria (85.6%), Tetrameres americana (80.8%), and Gongylonemaingluvicola (50.4%)[13]. Perminet al. (1999) carried out a cross-sectional prevalence study of gastrointestinal helminthes in Danish poultry production systems on 16 farms during1994 and 1995. In the free-range/organic systems the following helminthes were detected, A. galli (63.8%), H. gallinarum (72.5%), Capillaria obsignata (53.6%), Capillaria anatis (31.9%) and Capillaria caudinflata (1.5%)[16]. Bhat et al. (2014) in 600 fecal samples from poultry in northern India found A. galli (19.2%), H. gallinarus(9.5%), Capillaria sp. (3.5%), and Trichostrongylus tenuis (2.5%)[17]. In turn, Yazwinskiet al. (2013)in heavy layers from the southeast United States found an overall prevalence of 98.9%, and Heterakis gallinarum (96%), Capillariaobsignata(75%) and Ascaridiagalli (63%)[18]. In adult chickens from rural areas of Matebeleland Province, Zimbabwe, Dube et al. (2010) encountered Ascaridia galli, Heterakis gallinarum, H. dispar, and Capillaria annulata, as well as Tetrameres Americana, Acuaria hamulosa, and Allodapa suctoria [19].In Nigeria, Kolade and Agbolade (2014) examined 150 domestic fowls, consisting of 50 (20 males, 30 females) local and 100 (layers) exotic breeds and found a pooled prevalence of 66.7%. A. galli was the most prevalent and double infestations were minimal [20]. In another study on 133 (110 exotic and 23 local) domestic fowls from three locations in Nigeria,Agbolade et al. (2015) found an overall endoparasite frequency of 37.6% (50/133). The helminths recorded were Ascaridiagalli, Capillaria sp., Heterakis gallinarum, Syngamus trachea, hookworm, and Raillietina sp.[21]. Helminth parasites frequency by backyard All of the 14 chicken backyards resulted positive to helminth parasites. Four of them (4/14) were positive to the four species found (A. galli, Capillaria sp., Heterakis sp., T. tenuis).four (4/14) were positive to A. galli, Capillaria sp., and T. tenuis; three (3/14) were positive to A. galli, Capillaria sp. and Heterakis sp.), two (2/14) were positive to A. galli and Capillaria sp.; one (1/14) were positive to A. galli and Heterakis sp.). All backyards had birds affected by A. galli, 92.9%(13/14)had animals positive to Capillaria sp., and 57.1%(8/14) in each caseshowed poultry parasite by Heterakis sp. and byt. tenuis (Table-2). 465

Table-1. Positive samples of helminth parasites species found by backyard in Tembladeras Vista Hermosa, Oaxaca, Mexico. Backyard n A. galli Capillariasp. Heterakissp. T. tenuis A 35 22 0 2 0 B 11 4 2 0 0 C 8 4 4 1 0 D 21 7 8 7 5 E 15 4 5 0 0 F 20 9 8 7 1 G 20 8 10 0 2 H 20 11 6 1 10 I 15 5 5 2 0 J 15 1 1 0 1 K 15 3 4 0 2 L 20 5 8 0 6 M 25 10 8 14 0 N 30 13 9 17 6 Total 270 106 78 51 33 % positives/ 28.9 18.9 12.2 total 39.3 % positives/ 62.6 46.2 30.2 19.5 total of positives Helminth parasites frequency by age group and sex Table-3 summarizes the results of eggs per gram of gastrointestinal parasites disaggregated by stage and sex of birds. Independently of the stage, females had more positive cases mean and maximum eggs per gram counts than the males. Literature shows that eventually some host factors may cause variation in prevalence in some cases, but generally there is no significant difference in prevalence with respect to host sex. Also, the frequency of positives increased as birds aged, but it should be considered that older birds maybe are exposed longer to the contaminated environment than the chicks, hence a higher frequency rate. Table-3. Descriptive statistics of eggs per gram of poultry gastrointestinal parasites by stage and sex of birds in Tembladeras Vista Hermosa, Oaxaca, Mexico. Stage Sex Total Positives (%) Mean Std Dev. Minimum Maximum Grower Female 36 22(61.1) 131.9 221.1 0 1050 Grower Male 21 10(47.6) 100 183.7 0 800 Adult Female 138 97(70.3) 177.5 405 0 4150 Adult Male 32 20(62.5) 123.4 141.4 0 450 Chick 43 20(46.5) 102.3 191.47 0 950 Grower 57 32(56.1) 120.3 206.99 0 1050 Adult 170 117(68.8) 167.4 370.28 0 4150 Females 199 132(66.3) 164.3 359.55 0 4150 Males 71 37(52.1) 98.6 145.64 0 800 Andy-Chimbo(2014) in backyard poultry of Ecuador, obtained percentages of 50%, 58.42%, and 59.62% positive at stool examination, in relation to age (3-6, 7-12, > 12 months) respectively, but found 62% positive samples in males and41% in females[15], which is the opposite to the findings described in Table-3. 466

Table-4 shows how the species of gastrointestinal helminth parasites species is related to age and sex of birds. As in the general trend previously described, as bird ages the rate of parasite infection increases. In turn, except for Heterakissp., female tend to havea greater proportion of parasitized animals than males. Table-4. Positive samples by age and sex of birds and gastrointestinal helminth parasites species in Tembladeras Vista Hermosa, Oaxaca, Mexico. Age, months Total A. galli Capillariasp. Heterakissp. T. tenuis 1 a 2 43 14 (32.6)* a 7(16.3) a 6(13.9) a 2(4.7) a 2 a 8 57 20(35.1) a 13(22.8) b 9(15.8)a 2(3.5) a >8 170 72(42.4) b 58(34.1) c 36(21.2) b 29(17.1) b Sex Female 199 90(45.3) a 41(20.6)a 56(28.1) a 26(13.1) a Male 71 16(22.5) b 10(14.1) b 22(30.9) a 7(9.9) b * The number in parenthesis is the percentage value relative to the total in each category Dissimilar letter by column indicate statistical difference (p<0.05). In connection with the fecal eggcount, the overall average of eggs pergram of feces was 147±319. Female birds recorded a higher mean epg (164±359) compared to males (99±146) (p<0.05)the prevalence and incidence of gastrointestinal parasites affecting poultry may vary by diverse climatic and ecogeographic factors, as well as by the sanitary and hygienic conditions and the management practices. For instance, in Ethiopia, Reta (2009) found a higher helminthic parasite burden in mid altitude than in other agro-ecologies, indicating the relative suitability of parasite-environment interaction to successfully complete its life cycle in the mid-altitude than in other agroecologies [3]. In turn, Permin et al. (1999) concluded that there is a higher risk of helminth infections in free-range and backyard systems but prevalence may also be high in deep-litter systems [16]. Such parasite infections can lead to reduced growth rate, weight loss and decreased integrity of the intestinal mucosa, predisposing animals to secondary infections. According to Rodríguez-Vivas et al. (2001), Heterakis sp., A. galli and Capillaria sp. occur in flocks kept on floors, with wet beds, or defective drinking systems that allow water spillage[14]. The parasite species identified in this study are of direct cycle, their transmission is through contaminated soil and the infestation occurs orally by the ingestion of water and food contaminated with eggs. The feeding behavior of birds raise datliberty and the habit of birds to scratch the ground, are critical points inparasiticinfestation. Birds bred in the backyard everywhere are not free of risk for parasitic infections; furthermore, in a hot humid environment such as the one in which this study was conducted, it seems to be a direct and close relationship between the presences of parasitic agents and poor poultry management conditions. However, this study was conducted in the rainy season, when the intensity of parasitism is supposed to be higher, but more than a third of the sampled animals were negative. All chicken keepers are women. This seems to be a common feature in other parts of the world [22, 23, 24 24] (Alders 2012, Mandal et al. 2006, Simainga et al. 2010). There is a need to design and implement extension programs to support poultry owners and make them more knowledgeable and skillful about the recommended practices and new technologies so they and can maximize productivity and consequently their income. CONCLUSIONS An overall 62.6% of examined poultry were shedding nematode eggs in Tembladeras Vista Hermosa, Oaxaca, Mexico. All 14 chicken backyards examined had parasitized animals. Four types of gastrointestinal helminths were encountered,ascaridiagalli (62.6%), Capillariasp. (46.5%), Heterakis sp. (30.2%) and Trichostrongylus tenuis (19.5%). Mixed parasitism represented 42% of all cases of parasitism. Females had more positive cases to helminth infections(66.3%) than males (52.1%). The highest frequency of helminth infections was recorded in adults (68.8%), followed by growers (56.1%) and chicks (46.5%). Overall average of eggs per gram of feces was 147.04±318.6. Female birds recorded a significantly higher mean epg (164±359) compared to males (99±146). The present study sheds new light on the severity of the prevalence of gastrointestinal helminthic infections of backyard chickens of hot humid tropics in Mexico. More research is needed to identify all parasites in the region and the country, to understand the causes of infection, disease and death. It is also required to test integrated control strategies and to 467

improve chicken productivity and enhance smallholder livelihood in these areas. ACKNOWLEDGEMENTS The study was financed by Mexican Secretariat of Public Education (SEP) through a Professional Teaching Development Program (PRODEP) and University of Veracruz grant for the project Assessing and promoting family backyard poultry in central Veracruz, Mexico. The authors also thank the University of Veracruz for providing the work space and facilities, and farmers of Tembladeras Vista Hermosa, for their support, cooperation and willingness to collaborate in this project. REFERENCES [1] Branckaert R.D.S. andgueye E.F. 1999. FAO s Programme for Support to Family Poultry Production. Proceedings of the Workshop Poultry as a Tool in Poverty Eradication and Promotion of Gender Equality. Dolberg F and Petersen P H (editors), The Danish Agricultural and Rural Development Advisers' Forum, March 22-26, 1999, Tune Land boskole, Denmark. Retrieved from http://www.fao.org/docrep/004/ac154e/ac154e09.htm #ch5.4. [2] Finzi A. 2000. Integrated Backyard Systems. A contribution to the special programme for food security. Food and Agriculture Organization (FAO). Rome. Retrieved from http://www.fao.org/ag/againfo/themes/documents/ibys /. [3] Reta D. 2009. Understanding the role of indigenous chickens during the long walk to food security in Ethiopia. Livestock Res. Rural Dev. 21, Article #116.Retrieved from http://www.lrrd.org/lrrd21/8/dugu21116.htm. [4] Ruff M.D. 1999. Important parasites in poultry production systems. VeterinaryParasitology. 84(3-4): 337-347. [5] Magwisha H.B., Kassuku A.A., Kvysgaard N.C. andpermin A. 2002. A comparison of the prevalence and burdens of helminth infections in growers and adult free-range chickens Tropical Animal Health & Production. 34: 205-214. [6] Foreyt W.J.2002. Veterinary Parasitology. Reference Manual. 5a. ed., Iowa State University Press, Ames, IA. [7] Zajac A. andconboy G.A. (editors) 2012. Veterinary Clinical Parasitology. 8a. ed., Iowa State University Press, Ames, IA. [8] Thiepont D., Rochette F. andvanparijs O.F.J. 1986. Diagnosing Helminthiasis by Coprological examination. Janssen Research Foundation2nd ed. Beerse, The Netherlands. pp. 92-107. [9] Martin S.W., Meek A.H. and Willberg P. 1987. Veterinary Epidemiology, Principles and Methods, Iowa State University Press, Ames, Iowa. [10] Pattison M, McMullin P,, Bradbury J. and Alexander D. (Editors) 2008. Poultry diseases. 6 th ed. Saunders, Toronto. [11] Taylor M.A., Coop R.L. and Wall R.L. 2007. Veterinary Parasitology. 3a. ed., Wiley-Blackwell, Chicester, U K.Taylor MA, Coop RL, Wall RL 2007. Veterinary Parasitology. 3a. ed., Wiley-Blackwell, Chicester, U K. [12] Brugère-Picoux J., Vaillancourt J.P., Shivaprasad H.L., Venne D. and Bouzouaia M. 2015. Manual of Poultry Diseases. Association Française pour l' Avancement des Sciences, Paris. [13] Phiri I.K., Phiri A.M., Ziela M., Chota A,,Masuku M. and Monrad J. 2007. Prevalence and distribution of gastrointestinal helminths and their effects on weight gain in free-range chickens in Central Zambia. Tropical Animal Health Production. 39(4):309 315. [14] Rodríguez-Vivas R.I., Cob-Galera L.A., Domínguez- Alpizar J.L. 2001. Frequency of gastrointestinal parasites in domestic animals diagnosed in Yucatán, México. RevistaBiomédica. 12:19-25. [15] Andy-Chimbo C, R. 2014. Determination of major gastrointestinal parasites affecting backyard poultry (Gallus gallusdomesticus) in the El Descansocommunity, Canton Joya de los Sachas, Orellana Province. Thesis for Veterinary Medicine and Animal Science Degree. Faculty of Agricultural Sciences, Technical University of Ambato. Cevallos, Ecuador [In Spanish].Retrieved from http://repositorio.uta.edu.ec/bitstream/123456789/768 5/1/Tesis%2015%20Medicina%20Veterinaria%20y% 20Zootecnia%20-CD%20251.pdf. [16] Permin A., Bisgaard M., Frandsen F., Pearman M, & Nansen P. 1999. Prevalence of gastrointestinal 468

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