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Viability and development of Ascaridia galli eggs recovered in artificial media followed by storage under different conditions

Published online by Cambridge University Press:  13 October 2020

T. Feyera Open the ORCID record for T. Feyera [Opens in a new window] ,
I. Ruhnke ,
B. Sharpe ,
T. Elliott ,
D.L.M. Campbell  and
S.W. Walkden-Brown
T. Feyera*
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW2351, Australia Department of Veterinary Clinical Studies, College of Veterinary Medicine, Jigjiga University, P. O. Box 1020, Jigjiga, Ethiopia
I. Ruhnke
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW2351, Australia
B. Sharpe
Affiliation:
Invetus Pty Ltd, Armidale, NSW2350, Australia
T. Elliott
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW2351, Australia
D.L.M. Campbell
Affiliation:
Agriculture and Food, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Armidale, NSW2350, Australia
S.W. Walkden-Brown
Affiliation:
Animal Science, School of Environmental and Rural Science, University of New England, Armidale, NSW2351, Australia
*
Author for correspondence: T. Feyera, tdewo@myune.edu.au/tekafeye@gmail.com
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Abstract

Eggs oviposited by Ascaridia galli females in artificial media are commonly used as a source of infective material. We investigated the rate of egg production by cultured mature females (n = 223), and changes in egg viability under different storage and incubation conditions. Eggs recovered after 1, 2 or 3 days of culture were subjected to either (1) storage in water at 4°C (1, 4 or 8 weeks) followed by incubation in 0.1 N H2SO4 at 26°C (2, 4 or 6 weeks); or (2) prolonged storage at 4°C (up to 14 weeks). Egg development and viability was assessed by morphology coupled with a viability dye exclusion test of hatched larvae. Of the 6,044 eggs recovered per mature female 49.2, 38.5 and 12.3% were recovered on days 1, 2 and 3 of worm incubation respectively with similar initial viability (≥99%) between days. Eggs recovered on different days had only minor differences in viability after storage. The prolonged storage period at 4°C significantly affected both viability and embryonation ability resulting in decline in viability of 5.7–6.2% per week. A smaller but significant decline in egg (2.0%) and hatched larval (1.4%) viability per week of incubation at 26°C was also observed. We conclude that storage and incubation conditions, not the day of egg recovery, are the main factors affecting A. galli egg viability. Our findings indicate that under aerobic conditions storage at 26°C may be preferable to 4°C whereas other studies indicate that under anaerobic conditions storage at 4°C is preferable.

Keywords

embryonationhatched larvaenematodepoultrychicken
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e199
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Ackert, JE (1931) The morphology and life history of the fowl nematode Ascaridia lineata (Schneider). Parasitology 23, 360–379.CrossRefGoogle Scholar
Ackert, J, Cooper, RM and Dewhirst, L (1947) Viability of Ascaridia eggs under varying conditions of age and administration. Transactions of the American Microscopical Society 66, 383–389.CrossRefGoogle Scholar
Bottjer, KP, Bone, LW and Gill, SS (1985) Nematoda: susceptibility of the egg to Bacillus thuringiensis toxins. Experimental Parasitology 60, 239–244.CrossRefGoogle ScholarPubMed
Butler, RL and Christenson, RO (1942) A simple apparatus for determining the viability of embryonated helminth ova. The Journal of Parasitology 28, 131–134.CrossRefGoogle Scholar
Chadfield, M, Permin, A, Nansen, P and Bisgaard, M (2001) Investigation of the parasitic nematode Ascaridia galli (Shrank 1788) as a potential vector for Salmonella enterica dissemination in poultry. Parasitology Research 87, 317–325.CrossRefGoogle ScholarPubMed
Christenson, RO, Earle, H, Butler, RL and Creel, HH (1942) Studies on the eggs of Ascaridia galli and Heterakis gallinarum. Transactions of the American Microscopical Society 61, 191–205.CrossRefGoogle Scholar
Cruthers, L, Weise, RW and Hansen, M (1974) Topography of Ascaridia galli eggs exposed to low temperatures or cryoprotectants as shown by scanning electron microscopy. The Journal of Parasitology 60, 632–635.CrossRefGoogle ScholarPubMed
Dahl, C, Permin, A, Christensen, J, Bisgaard, M, Muhairwa, A, Petersen, KD, Poulsen, JD and Jensen, AL (2002) The effect of concurrent infections with Pasteurella multocida and Ascaridia galli on free range chickens. Veterinary Microbiology 86, 313–324.CrossRefGoogle ScholarPubMed
Daş, G, Kaufmann, F, Abel, H and Gauly, M (2010) Effect of extra dietary lysine in Ascaridia galli-infected grower layers. Veterinary Parasitology 170, 238–243.CrossRefGoogle ScholarPubMed
Daş, G, Hennies, M, Sohnrey, B, Rahimian, S, Wongrak, K, Stehr, M and Gauly, M (2017) A comprehensive evaluation of an ELISA for the diagnosis of the two most common ascarids in chickens using plasma or egg yolks. Parasites & Vectors 10, 187.CrossRefGoogle ScholarPubMed
Dick, JW, Leland, SE Jr and Hansen, M (1973) Hatching and in vitro cultivation of the nematode Ascaridia galli to the third-stage larva. Transactions of the American Microscopical Society 92, 225–230.CrossRefGoogle ScholarPubMed
Elliott, A (1954) Relationship of aging, food reserves, and infectivity of larvae of Ascaridia galli. Experimental Parasitology 3, 307–320.CrossRefGoogle ScholarPubMed
Ferdushy, T, Luna-Olivares, LA, Nejsum, P, Roepstorff, AK, Thamsborg, SM and Kyvsgaard, NC (2013) Population dynamics of Ascaridia galli following single infection in young chickens. Parasitology 140, 1078–1084.CrossRefGoogle ScholarPubMed
Gamboa, M (2005) Effects of temperature and humidity on the development of eggs of Toxocara canis under laboratory conditions. Journal of Helminthology 79, 327–331.CrossRefGoogle ScholarPubMed
Gauly, M, Bauer, C, Preisinger, R and Erhardt, G (2002) Genetic differences of Ascaridia galli egg output in laying hens following a single dose infection. Veterinary Parasitology 103, 99–107.CrossRefGoogle ScholarPubMed
Gauly, M, Homann, T and Erhardt, G (2005) Age-related differences of Ascaridia galli egg output and worm burden in chickens following a single dose infection. Veterinary Parasitology 128, 141–148.CrossRefGoogle ScholarPubMed
Hansen, M, Oonyawongse, R and Ackert, J (1953) Rate of development, viability, vigor, and virulence of Ascaridia galli ova cultured respectively in air and in water. The American Midland Naturalist 49, 743–750.CrossRefGoogle Scholar
Hørning, G, Rasmussen, S, Permin, A and Bisgaard, M (2003) Investigations on the influence of helminth parasites on vaccination of chickens against Newcastle disease virus under village conditions. Tropical Animal Health and Production 35, 415–424.CrossRefGoogle ScholarPubMed
Katakam, KK, Mejer, H, Dalsgaard, A, Kyvsgaard, NC and Thamsborg, SM (2014) Survival of Ascaris suum and Ascaridia galli eggs in liquid manure at different ammonia concentrations and temperatures. Veterinary Parasitology 204, 249–257.CrossRefGoogle ScholarPubMed
Katoch, R, Yadav, A, Godara, R, Khajuria, J, Borkataki, S and Sodhi, S (2012) Prevalence and impact of gastrointestinal helminths on body weight gain in backyard chickens in subtropical and humid zone of Jammu, India. Journal of Parasitic Diseases 36, 49–52.CrossRefGoogle ScholarPubMed
Kaufmann, F, Daş, G, Preisinger, R, Schmutz, M, König, S and Gauly, M (2011) Genetic resistance to natural helminth infections in two chicken layer lines. Veterinary Parasitology 176, 250–257.CrossRefGoogle ScholarPubMed
Kim, MK, Pyo, KH, Hwang, YS, Park, KH, Hwang, IG, Chai, JY and Shin, EH (2012) Effect of temperature on embryonation of Ascaris suum eggs in an environmental chamber. The Korean Journal of parasitology 50, 239–242.CrossRefGoogle Scholar
Luna-Olivares, LA, Ferdushy, T, Kyvsgaard, NC, Nejsum, P, Thamsborg, SM, Roepstorff, A and Iburg, TM (2012) Localization of Ascaridia galli larvae in the jejunum of chickens 3 days post infection. Veterinary Parasitology 185, 186–193.CrossRefGoogle ScholarPubMed
Mero, WM and Gazal, A (2008) Effect of constant and changing temperatures on the development and viability of Ascaridia galli eggs. Paper presented at the 2nd Kurdistan Conference on Biological Sciences. Journal of Duhok University 12, 35–38.Google Scholar
Onyirioha, J (2011) Effects of varying temperatures on the ex-uterine development and incubation period of eggs of Ascaridia galli. New York Science Journal 4, 61–63.Google Scholar
Permin, A and Hansen, J (1998) Epidemiology, diagnosis and control of poultry parasites. FAO Animal Health Manual 4, 24–29.Google Scholar
Permin, A, Bojesen, M, Nansen, P, Bisgaard, M, Frandsen, F and Pearman, M (1997a) Ascaridia galli populations in chickens following single infections with different dose levels. Parasitology Research 83, 614–617.CrossRefGoogle Scholar
Permin, A, Pearman, MAG, Nansen, P, Bisgaard, M and Frandsen, FN (1997b) An investigation on different media for embryonation of Ascaridia galli eggs. Helminthologia 34, 75–79.Google Scholar
Permin, A, Christensen, JP and Bisgaard, M (2006) Consequences of concurrent Ascaridia galli and Escherichia coli infections in chickens. Acta Veterinaria Scandinavica 47, 43–54.CrossRefGoogle ScholarPubMed
Phiri, I, Phiri, A, 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 and Production 39, 309–315.CrossRefGoogle ScholarPubMed
Pleidrup, J, Dalgaard, TS, Norup, LR, et al. (2014) Ascaridia galli infection influences the development of both humoral and cell-mediated immunity after Newcastle disease vaccination in chickens. Vaccine 32, 383–392.CrossRefGoogle ScholarPubMed
Rahimian, S, Gauly, M and Daş, G (2016) Embryonation ability of Ascaridia galli eggs isolated from worm uteri or host faeces. Veterinary Parasitology 215, 29–34.CrossRefGoogle ScholarPubMed
Ramadan, HH and Abouznada, NY (1992) Morphology and life history of Ascaridia galli in the domestic fowl that are raised in Jeddah. Journal of King Abdulaziz University - Science 4, 87–99.CrossRefGoogle Scholar
Reid, WM (1960) Effects of temperature on the development of the eggs of Ascaridia galli. Journal of Parasitology 46, 63–67.CrossRefGoogle Scholar
Ruhnke, I, Andronicos, NM, Swick, RA, Hine, B, Sharma, N, Kheravii, SK, Wu, SB and Hunt, P (2017) Immune responses following experimental infection with Ascaridia galli and necrotic enteritis in broiler chickens. Avian Pathology 46, 602–609.CrossRefGoogle ScholarPubMed
Salih, NE and Saleem, KM (1987) In vitro hatching of the infective eggs of Ascaridia galli in tissue extracts. Veterinary Parasitology 24, 263–268.CrossRefGoogle ScholarPubMed
Shafir, SC, Sorvillo, FJ, Sorvillo, T and Eberhard, ML (2011) Viability of Baylisascaris procyonis eggs. Emerging Infectious Diseases 17, 1293–1295.CrossRefGoogle ScholarPubMed
Sharma, N, Hunt, P, Hine, B, Sharma, N, Swick, R and Ruhnke, I (2017) Ascaridia galli challenge model in laying hens. Journal of Advances in Parasitology 4, 41–46.Google Scholar
Sharma, N, Hunt, PW, Hine, BC, Sharma, NK, Swick, RA and Ruhnke, I (2018) Detection of Ascaridia galli infection in free-range laying hens. Veterinary Parasitology 256, 9–15.CrossRefGoogle ScholarPubMed
Soulsby, E (1982) Helminths, arthropods and protozoa of domesticated animals. 7th edn. 906 p. London, UK, Bailliere Tindall.Google Scholar
Tarbiat, B, Jansson, DS and Höglund, J (2015) Environmental tolerance of free-living stages of the poultry roundworm Ascaridia galli. Veterinary Parasitology 209, 101–107.CrossRefGoogle ScholarPubMed
Tarbiat, B, Rahimian, S, Jansson, D, Halvarsson, P and Höglund, J (2018) Developmental capacity of Ascaridia galli eggs is preserved after anaerobic storage in faeces. Veterinary Parasitology 255, 38–42.CrossRefGoogle ScholarPubMed
Taylor, M, Coop, R and Wall, R (2007) Parasites of poultry and gamebirds. Veterinary Parasitology 3, 459–557.Google Scholar
Terrill, T, Larsen, M, Samples, O, Husted, S, Miller, J, Kaplan, R and Gelaye, S (2004) Capability of the nematode-trapping fungus Duddingtonia flagrans to reduce infective larvae of gastrointestinal nematodes in goat feces in the southeastern United States: dose titration and dose time interval studies. Veterinary Parasitology 120, 285–296.CrossRefGoogle ScholarPubMed
Thapa, S, Meyling, NV, Katakam, KK, Thamsborg, SM and Mejer, H (2015b) A method to evaluate relative ovicidal effects of soil microfungi on thick-shelled eggs of animal-parasitic nematodes. Biocontrol Science and Technology 25, 756–767.CrossRefGoogle Scholar
Thapa, S, Thamsborg, SM, Meyling, NV, Dhakal, S and Mejer, H (2017) Survival and development of chicken ascarid eggs in temperate pastures. Parasitology 144, 1243–1252.CrossRefGoogle ScholarPubMed
Thapa, S, Hinrichsen, LK, Brenninkmeyer, C, et al. (2015a) Prevalence and magnitude of helminth infections in organic laying hens (Gallus gallus domesticus) across Europe. Veterinary Parasitology 214, 118–124.CrossRefGoogle Scholar
Thienpont, D, Rochette, F and Vanparijs, OFJ (1986) Diagnosing helminthiasis by coprological examination. 2nd edn. 35–36 pp. Beerse, Belgium, Janssen Research Foundation.Google Scholar
Tian, B, Yang, J and Zhang, KQ (2007) Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiology Ecology 61, 197–213.CrossRefGoogle ScholarPubMed
Tiersch, K, Daş, G, Samson-Himmelstjerna, GV and Gauly, M (2013) The role of culture media on embryonation and subsequent infectivity of Capillaria obsignata eggs. Parasitology Research 112, 357–364.CrossRefGoogle ScholarPubMed
Todd, A, Crowdus, D and Wyant, Z (1952) Experimental embryonation of the egg and development of Ascaridia galli in its chicken host. Experimental Parasitology 1, 176–183.CrossRefGoogle Scholar
Wharton, D (1980) Nematode egg-shells. Parasitology 81, 447–463.CrossRefGoogle ScholarPubMed
Whitlock, H (1948) Some modifications of the McMaster helminth egg-counting technique and apparatus. Journal of the Council for Scientific and Industrial Research 21, 177–180.Google Scholar
Wongrak, K, Gauly, M and Daş, G (2015) Diurnal fluctuations in nematode egg excretion in naturally and in experimentally infected chickens. Veterinary Parasitology 208, 195–203.CrossRefGoogle ScholarPubMed
Wuthijaree, K, Lambertz, C and Gauly, M (2017) Prevalence of gastrointestinal helminth infections in free-range laying hens under mountain farming production conditions. British Poultry Science 58, 649–655.CrossRefGoogle ScholarPubMed