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An Outbreak of Intestinal Obstruction by Ascaridia Galli in Broilers in Minas Gerais

ABSTRACT

Industrial broilers raised on helminthic medication-free feed were diagnosed with a severe disease caused by Ascaridia galli, characterized by intestinal hemorrhage and obstruction. A. galli was identified based on the morphological features of the nematode. Broilers were raised for a longer period (63 days) for weight recovery, grouped as stunted (n=500), had low body score and had fetid diarrhea. The duodenum-jejunum segment was the most severely affected with obstruction and had localized accumulation of gas. The intestinal mucosa was severely congested with petechial and suffusive hemorrhages. The outbreak resulted in morbidity of about 10% and mortality of up to 4% and was associated to the absence of preventive medication on feed and slack biosecurity. The reemergence of A. galli is discussed in view of the alternative poultry management and raising conditions for drug free and welfare.

Keywords:
Ascaroidea; broiler chicken; nematode; enteriitis

INTRODUCTION

Ascaridia galli is returning to the relevant poultry diseases scene as alternative free-range broilers and cage-free layer chickens are progressively in higher demand by consumers. Floor and ground conditions enable the direct ingestion of eggs or larvae or mechanical vectors of Ascaridia galli, such as earthworms, which may concentrate and protect eggs (Augustine, 1974), although the transmission is mainly direct and the life cycle simple. Eggs develop infective larvae within about 12 days and are resistant to cold. The normal development and viability of A. galli eggs is highest in anaerobic conditions in feces at cold temperatures but lowest in feces or water at warmer temperatures, as eggs maintained in normal embryogenesis with little loss of viability in feces at 4°C, but with large viability losses in clean water at 25°C (Tarbiat et al., 2018Tarbiat B, Rahimian S, Jansson DS, Halvarsson P, Höglund J. Developmental capacity of Ascaridia galli eggs is preserved after anaerobic storage in faeces. Veterinary Parasitology 2018;255:38-42.). Infection will result in reduced productive performance of meat or eggs, and high parasitic load will cause intestinal blood loss, increased mortality, and anemia, and may aggravate other conditions (Norton & Ruff, 2003).

In Germany, cage-free organic layers were shown to harbor, mostly subclinically, the nematodes Ascaridia galli (88%), Heterakis gallinarum (98%), and Capillaria spp (75.3%) (Kaufmann et al., 2011Kaufmann F, Das G, Sohnrey B, Gauly M. Helminth infections in laying hens kept in organic free range systems in Germany. Livestock Science 2011;141:182-187.). In Sweden, layers are challenged with genetically related Ascaridia galli strains, indicating recent and stationary flock infections (Höglund et al., 2012Höglund J, Morrison DA, Engström A, Nejsum P, Jansson DS. Population genetic structure of Ascaridia galli re-emerging in non-caged laying hens. Parasites & Vectors. 2012;5:97.). A more extensive study in eight European countries investigated helminthic infection, revealing A. galli with an overall prevalence of 69.5%, and that, in contrast to the general assumption, the outdoor pasture did not correlate to the infection (Thapa et al., 2015Thapa S, Hinrichsen LK, Brenninkmeyer C, Gunnarsson S, Heerkens JL, Verwer C, et al. Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 2015;214:118-224.).

In Brazil (São Paulo), adult chickens of different housing and management strategies, were shown most commonly infected by A. galli and Heterakis gallinarum (Silva et al., 2016Silva GS, Romera DM, Fonseca LEC, Meireles MV. Helminthic parasites of chickens (Gallus domesticus) in different regions of São Paulo State, Brazil. Brazilian Journal of Poultry Science 2016;18(1):163-168.). An outbreak of intestinal disease in Pavo cristatus causing diarrhea, dehydration, anorexia and weight loss, was associated to A. galli (Teixeira et al., 2012Teixeira M, Monteiro JP, Catenacci LS, Azevedo Rodrigues MD, Carvalho M. Ascaridiasis in peafowl Pavo cristatus (Phasianidae) due to Ascaridia galli Schrank, 1788. Journal of Zoo and Wildlife Medicine 2012;43(3):585-587.). Wild native and exotic domestic avian species were investigated for the presence of endoparasites in feces and found A. galli in Buteo magnirostris and P. cristatus (Marietto-Gonçalves et al., 2009Marietto-Gonçalves GA, Martins TF, Lima ET, Souza Lopes R, Andreatti Filho RL. Prevalência de endoparasitas em amostras fecais de aves silvestres e exóticas examinadas no Laboratório de Ornitopatologia e no Laboratório de Enfermidades Parasitárias da FMVZ-UNESP/Botucatu-SP. Ciência Animal Brasileira 2009;10(1):349-354.; Andery et al., 2013Andery DA, Ferreira Junior FC, Araújo AV, Vilela DAR, Marques MVR, Marín SY, et al. Health assessment of raptors in triage in Belo Horizonte, MG, Brazil. Brazilian Journal of Poultry Science 2013;15(3):247-256.).

This manuscript aims to report an outbreak of severe infection by Ascaridia galli resulting in intestinal hemorrhage and obstruction and high mortality of industrial broilers raised on medication-free feed.

MATERIALS AND METHODS

Broilers (n=4) which were raised up to nine weeks of age were received for diagnosis, with history of morbidity of approximately 10% and mortality of approximately 4%. The flock was formed by gathering stunted chicks for separate management and characterized by low performance, stunted growth and low body weight. All birds in the sample were chosen considering the stunted growth. Broilers were raised on balanced nutrient but helminthic medication-free diet, with a total of 500 birds in the flock. Housing was in conventional brick house for industrial broilers, with industrial grade feeders and drinkers, forced ventilation, curtains, cemented floor and wood shavings bedding. However, biosecurity was not effective, without entrance control, allowing visitation, with no footbath or vehicle disinfection. Complete necropsies were performed, and nematodes collected, processed, mounted as described previously (Bowman, 2009Bowman DD. Georgis' parasitology for veterinarians. 9th ed. Philadelphia: Saunders Elsevier; 2009.), and identified according to the morphology and micrometry (Soulsby, 1982Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. 7th ed. London: Bailliere Tindall; 1982. p.164-175.). Briefly, nematodes were immersed in warm buffered saline (PBS pH 7.4) and within a few minutes were subsequently transferred to a buffered formaline solution (formaldehyde 10% in PBS). Helminths were diaphanized in lactophenol (20% phenic acid, 20% lactic acid, 40% glycerine; 20% distilled water) and mounted onto glass slides with coverslip in melt phenol gelatin (10g gelatin; 60mL distillled water; 70ml glycerine; 0.5mL phenic acid) and visualized with an optical microscopy (Olympus B-H2) at 40 and 100 magnifications.

RESULTS AND DISCUSSION

Broilers were described with chronic fluid fetid diarrhea and showed low body score for the age, with prominent carina (sternum), as a result of reduced pectoral mass. Enlarged intestines with gas accumulations were seen at necropsy, where Ascaridia galli concentrated, mostly at the cranial part of the jejunum, causing obstruction and mucosal congestion (Fig. 1). The microscopic aspects of the morphology of A. galli adults and eggs are shown (Fig. 2).

Figure 1
A: Small intestines of broiler chicken. Intestinal segments are enlarged and with accumulations of gas (arrows), as a result of obstructions by Ascaridia galli, especially at the cranial part of jejunum. B: High burden of Ascaridia galli with congested mucosa (arrow) in the jejunum.

Figure 2
Ascaridia galli 2A and 2B: Eggs; Note that eggs are characterized by a thick shell; 2C: Lateral view of the buccal apparatus of male; 2D: Frontal view of the buccal entrance of a male, showing three-independent lips. 2E: Ventral view of the male reproductive organs; the spicule is visible (arrow); 2F: Lateral view of the female caudal end, with the anus visible (arrow).

Ascaridia infections are known to be rare in caged chickens, including welfare cages, but common in non-caged systems, as here described for indoor broilers. In the outbreak here described, broilers were raised in conventional houses, but without adequate biosecurity, such as entrance control for visitors or vehicle disinfection, and were given feed with no anthelminthic medication. The improvement of management factors such as housing, litter and nutritional quality, schedule times of opening and closing popholes, alternation of pasture and supply of required materials may have a role in the reduction of the helminthic load (Thapa et al., 2015Thapa S, Hinrichsen LK, Brenninkmeyer C, Gunnarsson S, Heerkens JL, Verwer C, et al. Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 2015;214:118-224.), as free-range conditions enable the ingestion of eggs or larvae, or mechanical vectors of Ascaridia galli, such as earthworms (Augustine, 1974). Although free-range on grass did not correlate to Ascaridia galli infection in Europe (Thapa et al., 2015), despite temperatures of 18.8°C or lower will stop larva development (Reid, 1960Reid WM. Effects of temperature on the development of the eggs of Ascaridia galli. The Journal of Parasitology 1960;46(1):63-67.), but preserving its viability (Tharbiat et al., 2018), the climatic and environmental conditions may have a role in other regions, such as cooler climates. A. galli has a broad avian host range and infection has been described in industrial and free-range chickens, and wild species (Marietto-Gonçalves et al., 2009Marietto-Gonçalves GA, Martins TF, Lima ET, Souza Lopes R, Andreatti Filho RL. Prevalência de endoparasitas em amostras fecais de aves silvestres e exóticas examinadas no Laboratório de Ornitopatologia e no Laboratório de Enfermidades Parasitárias da FMVZ-UNESP/Botucatu-SP. Ciência Animal Brasileira 2009;10(1):349-354.; Silva et al., 2016Silva GS, Romera DM, Fonseca LEC, Meireles MV. Helminthic parasites of chickens (Gallus domesticus) in different regions of São Paulo State, Brazil. Brazilian Journal of Poultry Science 2016;18(1):163-168.; Teixeira et al., 2012Teixeira M, Monteiro JP, Catenacci LS, Azevedo Rodrigues MD, Carvalho M. Ascaridiasis in peafowl Pavo cristatus (Phasianidae) due to Ascaridia galli Schrank, 1788. Journal of Zoo and Wildlife Medicine 2012;43(3):585-587.; Andery et al., 2013Andery DA, Ferreira Junior FC, Araújo AV, Vilela DAR, Marques MVR, Marín SY, et al. Health assessment of raptors in triage in Belo Horizonte, MG, Brazil. Brazilian Journal of Poultry Science 2013;15(3):247-256.).

Lesions by A. galli will harm intestinal function and performance, with retarded growth and production (Daş et al., 2012), especially by larval stages (Luna-Olivares et al., 2015Luna-Olivares LA, Kyvsgaard NC, Ferdushy T, Nejsum P, Thamsborg SM, Roepstorff A, et al. The jejunal cellular responses in chickens infected with a single dose of Ascaridia galli eggs. Parasitology Research 2015;114:2507-2515.), as here observed as intestinal hemorrhages and obstruction.

The introduction of Ascaridia galli infection in the premises might be associated to infected replacement chickens (Höglund et al., 2011Höglund J, Jansson DS. Infection dynamics of Ascaridia galli in non-caged laying hens. Veterinary Parasitology 2011;180:267-273.), although the established infection will maintain a local genetic profile identity, and with genetic variations among farms (Höglund et al., 2012). Broilers in the present outbreak were raised in premises without entrance control, hence insufficient biosecurity. Visitor entry to the house or unit is a management error which results in eggs introduced horizontally into the farms (Jansson et al., 2010Jansson DS, Nyman A, Vågsholm I, Christensson D, Göransson M, Fossum O, et al. Ascarid infections in laying hens kept in different housing systems. Avian Pathology 2010;39(6):525-32.).

Ascaridiosis seems to be reemerging in several countries due to alternative raising or housing. In Serbia, hens of organic egg production were found 15.6-24.0% positive for A. galli (Tamara et al., 2019). In Argentina, broiler chicken flocks were evaluated and 25% of flocks were shown infected but no correlation was found between nematodes and coccidian infections (De Franceschi et al., 2008Franceschi ME, Barrios HA, Filippini OS. Association between coccidia and intestinal helminths in broiler chickens. International Journal of Poultry Science 2008;7(1):36-9.). Previous studies in Brazil, have found broiler flocks infected by Ascaridia galli in 10/17 municipalities of São Paulo (Da Silva et al., 2018Silva GS, Romera DM, Silva Conhalato G, Soares VE, Meireles MV. Helminth infections in chickens (Gallus domesticus) raised in different production systems in Brazil. Veterinary Parasitology: Regional Studies and Reports 2018;12:55-60.), in free-range flocks in the neighboring state (Paraná), with 45% infected (Vieira et al., 2015Vieira FE, Yamamura MH, Freire RL, Headle SA. The effects of managerial systems on helminth infection in free-range chickens from northern Paraná, Brazil. Semina: Ciências Agrárias 2015;36(2):4311-4322.), and in Santa Catarina in 21.7% (Quadros et al., 2015Quadros RM, Wiggers SB, Paes MP, Marques SM. Prevalência de endo e ectoparasitos de galinhas caipiras em pequenas propriedades da região serrana de Santa Catarina. Pubvet 2015;9:1-51.). In our study, we show that raising broilers in Minas Gerais, previously shown to naturally occur A galli by Mendes et al. (1976Mendes MD, Rocha Woelz C, Abdalla SI. Investigação copro-parasitológica em aves (Gallus gallus L., 1758), naturalmente infestadas, na região de Campo Florido, Minas Gerais, Brasil. Revista da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo 1976;13(1):213-217.) and in our unpublished extension service, especially for longer and without preventive medication, may lead to highly significant infection.

The information available on the affected flock revealed the strategic use of mebendazole for treatment against ascaridiasis. However, more effective drugs have been recommended against A. galli, such as fenbendazole, dl-tetramizole, levamizole or pyrantel tartrate (Norton & Ruff, 2003), none of which are permitted in drug-free poultry.

The climatic conditions and change in Brazil may favor parasitism in most of the Brazilian territory, with the survival of eggs in feces, especially at cooler temperatures (Tharbiat et al., 2018). The adoption of medication-free diet will demand for frequent fecal monitoring and strict biosecurity, in order to reduce the risk of helminthiasis. However, the use of antihelmintics has been considered a selective pressure for resistance. For instance, the subtherapeutic preventive dosage with benzimidazole has been involved in resistance by Ostertagia ostertagi in bovines (Knapp-Lawitzke et al. 2015Knapp-Lawitzke F, Krücken J, Ramünke S, Von Samson- Himmelstjerna G, Demeler J. Rapid selection for ?- tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture. Veterinary Parasitology 2015;209:84-92.).

CONCLUSIONS

The parasitism by Ascaridia galli in broilers is a growing concern worldwide, especially for alternative poultry, or in drug-free raising of broilers, as shown here. The growth of industrial broilers in medication-free diets will demand for all the adequate preventive veterinary medicine measures to be taken.

REFERENCES

  • Andery DA, Ferreira Junior FC, Araújo AV, Vilela DAR, Marques MVR, Marín SY, et al. Health assessment of raptors in triage in Belo Horizonte, MG, Brazil. Brazilian Journal of Poultry Science 2013;15(3):247-256.
  • Bowman DD. Georgis' parasitology for veterinarians. 9th ed. Philadelphia: Saunders Elsevier; 2009.
  • Das G, Abel H, Rautenschlein S, Humburg J, Schwarz A, Breves G, et al. The effects of dietary non-starch polysaccharides on Ascaridia galli infection in grower layers. Parasitology 2012;139:110-119.
  • Silva GS, Romera DM, Silva Conhalato G, Soares VE, Meireles MV. Helminth infections in chickens (Gallus domesticus) raised in different production systems in Brazil. Veterinary Parasitology: Regional Studies and Reports 2018;12:55-60.
  • Franceschi ME, Barrios HA, Filippini OS. Association between coccidia and intestinal helminths in broiler chickens. International Journal of Poultry Science 2008;7(1):36-9.
  • Höglund J, Morrison DA, Engström A, Nejsum P, Jansson DS. Population genetic structure of Ascaridia galli re-emerging in non-caged laying hens. Parasites & Vectors. 2012;5:97.
  • Höglund J, Jansson DS. Infection dynamics of Ascaridia galli in non-caged laying hens. Veterinary Parasitology 2011;180:267-273.
  • Jansson DS, Nyman A, Vågsholm I, Christensson D, Göransson M, Fossum O, et al. Ascarid infections in laying hens kept in different housing systems. Avian Pathology 2010;39(6):525-32.
  • Kaufmann F, Das G, Sohnrey B, Gauly M. Helminth infections in laying hens kept in organic free range systems in Germany. Livestock Science 2011;141:182-187.
  • Knapp-Lawitzke F, Krücken J, Ramünke S, Von Samson- Himmelstjerna G, Demeler J. Rapid selection for ?- tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture. Veterinary Parasitology 2015;209:84-92.
  • Luna-Olivares LA, Kyvsgaard NC, Ferdushy T, Nejsum P, Thamsborg SM, Roepstorff A, et al. The jejunal cellular responses in chickens infected with a single dose of Ascaridia galli eggs. Parasitology Research 2015;114:2507-2515.
  • Marietto-Gonçalves GA, Martins TF, Lima ET, Souza Lopes R, Andreatti Filho RL. Prevalência de endoparasitas em amostras fecais de aves silvestres e exóticas examinadas no Laboratório de Ornitopatologia e no Laboratório de Enfermidades Parasitárias da FMVZ-UNESP/Botucatu-SP. Ciência Animal Brasileira 2009;10(1):349-354.
  • Mendes MD, Rocha Woelz C, Abdalla SI. Investigação copro-parasitológica em aves (Gallus gallus L., 1758), naturalmente infestadas, na região de Campo Florido, Minas Gerais, Brasil. Revista da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo 1976;13(1):213-217.
  • Quadros RM, Wiggers SB, Paes MP, Marques SM. Prevalência de endo e ectoparasitos de galinhas caipiras em pequenas propriedades da região serrana de Santa Catarina. Pubvet 2015;9:1-51.
  • Reid WM. Effects of temperature on the development of the eggs of Ascaridia galli. The Journal of Parasitology 1960;46(1):63-67.
  • Silva GS, Romera DM, Fonseca LEC, Meireles MV. Helminthic parasites of chickens (Gallus domesticus) in different regions of São Paulo State, Brazil. Brazilian Journal of Poultry Science 2016;18(1):163-168.
  • Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. 7th ed. London: Bailliere Tindall; 1982. p.164-175.
  • Tarbiat B, Rahimian S, Jansson DS, Halvarsson P, Höglund J. Developmental capacity of Ascaridia galli eggs is preserved after anaerobic storage in faeces. Veterinary Parasitology 2018;255:38-42.
  • Teixeira M, Monteiro JP, Catenacci LS, Azevedo Rodrigues MD, Carvalho M. Ascaridiasis in peafowl Pavo cristatus (Phasianidae) due to Ascaridia galli Schrank, 1788. Journal of Zoo and Wildlife Medicine 2012;43(3):585-587.
  • Thapa S, Hinrichsen LK, Brenninkmeyer C, Gunnarsson S, Heerkens JL, Verwer C, et al. Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 2015;214:118-224.
  • Vieira FE, Yamamura MH, Freire RL, Headle SA. The effects of managerial systems on helminth infection in free-range chickens from northern Paraná, Brazil. Semina: Ciências Agrárias 2015;36(2):4311-4322.

Publication Dates

  • Publication in this collection
    20 Dec 2019
  • Date of issue
    2019

History

  • Received
    13 Apr 2019
  • Accepted
    29 Oct 2019
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