Experimental Salmonella Gallinarum infection in point of lay pullets: Correlation of hematology and oxidative stress with egg production https://doi.org/10.12982/VIS.2025.073
Main Article Content
Abstract
Salmonella Gallinarum is a bacterial pathogen linked with drop in egg production in poultry. In this study, hematological and oxidative stress (OS) parameters were evaluated and correlated with egg production in point of lay (POL) pullets infected with S. Gallinarum. Fifty 18-week-old POL pullets were randomly assigned to two groups of 25 POL pullets per group. The infected POL pullets were orally inoculated with S. Gallinarum (109S. Gallinarum colony forming units/mL), while the uninfected pullets were the controls. Hematological and OS parameters were determined using standard methods. There were significant (P < 0.05) loss of body weight and drop in egg production in the infected POL pullets when compared to the controls. Acute hemolytic anemia of the macrocytic hypochromic type was observed. The total white blood cell (TWBC), absolute heterophil, lymphocyte, eosinophil and monocyte counts, mean serum malondialdehyde (MDA) level, glutathione peroxidase (GPx), superoxide dismutase (SOD) and catalase (CAT) activities were significantly (P < 0.05) higher in the infected POL pullets when compared to the controls. There was a strong association between heterophilia and drop in egg production. An association was also established between significantly elevated GPx, SOD and CAT, which have antioxidant properties, and clinical outcome, including subsequent weight gain and rise in egg production, suggesting that antioxidants may be useful in the treatment of fowl typhoid. It was concluded that S. Gallinarum infection of POL pullets caused significant hematological changes, induced OS, and stimulated the body’s antioxidant defense mechanism to elaborate GPx, SOD and CAT.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Assoku, R.K., Penhale, W.J., 1978. The anaemia in fowl typhoid: Immmuno-pathogenesis and associated patterns of erythrocyte destruction. J. Comp. Pathol. 88, 219-236.
Baldrey, V., 2012. Interpreting blood profiles in avian. Available online: https//www.vettimes.co.uk.
Barbour, E.K., Ayyash, D.B., Alturkistni, W., Alyahiby, A., Yaghmoor, S., Iyer, A., Yousef, J., Kumosani, T., Harakeh, S., 2015. Impact of sporadic reporting of poultry Salmonella serovars from selected developing countries. J. Infect. Dev. Countries. 9, 1-7.
Berchieri, Jr. A., Murphy, C.K., Marston, K., Barrow, P.A., 2001. Observations on the persistence and vertical transmission of Salmonella enterica serovars Pullorum and Gallinarum in chickens: effect of bacterial and host genetic background. Avian Pathol. 30(1), 221-231.
Berchieri, Jr. A., Oliveira, G.H., Pinheiro, L.A.S., Barrow, P.A., 2000. Experimental Salmonella Gallinarum infection in light laying hen lines. Braz. J. Microbiol. 31(1), 50-52.
Beyaz, L., Atasever, A., Aydin, F., Gumusoy, K.S., Abay, S., 2010. Pathological and clinical findings and tissue distribution of Salmonella Gallinarum infection in Turkey poults. Turk. J. Vet. Anim. Sci. 34(2), 101-110.
Bizoń, A., Chojdak-Łukasiewicz, J., Budrewicz, S., Pokryszko-Dragan, A., Piwowar, A., 2023. Exploring the relationship between antioxidant enzymes, oxidative stress markers, and clinical profile in relapsing-remitting multiple sclerosis. Antioxidants. 12(8), 1638.
Campbell, T.W., 1994. Hematology. In: Ritchie, B.W., Harrison, G.J., Harrison, L.R. (Eds.), Avian medicine: principles and application. Wingers Publishing, Lake Worth, Florida, U.S.A, pp. 176-198.
Campbell, T.W., Ellis, C.K., 2007. Hematology of birds. In: Campbell, T.W., Ellis, C.K. (Eds.), Avian hematology and cytology, (3rd edition). Blackwell, Ames, pp. 3-50.
Chickipedia, 2019. Health and biosecurity: what is a healthy hen? Available online: https://hn-int.com/health-biosecurity/.
Chiroma, M.A., Adamu, S., Gadzama, J.J., Esievo, K.A.N., Abdulsalam, H., Sani, N.A., Joshua, L., Muhammad, Y., 2017. Hematological changes in layers experimentally infected with Salmonella Gallinarum. Afr. J. Cell. Pathol. 8, 36-42.
Chitty, J., 2018. Sample taking and basic clinical pathology. In: Chitty, J., Monks, D. (Eds.), BSAVA manual of avian practice. British Small Animal Veterinary Association, Gloucestershire, pp. 172-186.
Christensen, J.P., Barrow, P.A., Olsen, J.E., Poulsen, J.S.D., Bisgaard, M., 1996. Correlation between viable counts of Salmonella Gallinarum in spleen and liver and the development of anemia in chickens as seen in experimental fowl typhoid. Avian Pathol. 25, 769-783.
Draper, H.H., Hadley, M., 1990. Malondialdehyde determination as an index of lipid peroxidation. Meth. Enzymol. 186, 421-431.
English, K., 2008. Assessment of avian anemia. Available online: https//www.vettimes.co.uk.
Ezema, W.S., Onuoha, E., Chah, K.F., 2009. Observations on an outbreak of fowl typhoid in commercial laying birds in Udi, South Eastern Nigeria. Comp. Clin. Pathol. 18(4), 395-398.
Feldmann, B.V., Zinki, J.G., Jain, N.C., 2000. Shalm's veterinary hematology, 5th edition. Lea and Fibiger, Philadelphia, USA.
Freitas-Neto, O.C., Arroyave, W., Alessi, A.C., Fagliari, J.J., Berchier, Jr. A., 2007. Infection of commercial laying hens with Salmonella Gallinarum: Clinical, anatomopathological and hematological studies. Braz. J. Poult. Sci. 9(2), 133-141.
Galovicova, L., Borotova, P., Vukovic, N.L., Vukic, M., Kunova, S., Hanus, P., Kowalczewski, P.L., Bakay, L., Kacaniova, M., 2022. The potential use of Citrus aurantifolia L. Essential oils for decay control, quality preservation of Agricultural products, and anti-insect activity. Agronom. 12, 735.
Garcia, K.O., Santana, A.M., Freitas, Neto, O.C., Berchieri, Jr. A., Fagliari, J.J., 2010. Experimental infection of commercial layers using a Salmonella enterica serovar Gallinarum strain: blood serum component and histopathological changes. Braz. J. Vet. Pathol. 3(2), 111-117.
Gonzales, R., Auclair, C., Voison, E., Gautero, H., Dhermy, D., Boivin, P.,1984. Superoxide dismutase, catalase and glutathione peroxidase in red blood cells from patients with malignant diseases. Cancer Res. 44, 4137-4139.
Gutteridge, J., Halliwell, B., 2000. Free radicals and antioxidants in the year 2000: a historical look to the future. Ann. N. Y. Acad. Sci. 899, 126-147.
Haque, A.K.M.Z., Akter, M.R., Islam, S.S., Alam, J., Neogi, S.B., Yamasaki, S., Kabir, S.M.L., 2021. Salmonella Gallinarum in small-scale commercial layer flocks: Occurrence, molecular diversity and antibiogram. Vet. Sci. 8, 71.
Higgins, T., Beutler, E., Doumas, B.T., 2008. Measurement of hemoglobin in blood. In: Burtis, C.A., Ashwood, E.R., Bruns, D.E. (Eds), Tietz fundamentals of clinical chemistry, (6th edition). Sanders Elsevier, Missouri, pp. 524-525.
Hoque, M.N., Mohiuddin, R.B., Khan, M.M.H., Hannan, A., Alam, M.J., 2019. Outbreak of Salmonella in poultry of Bangladesh and possible remedy. J. Adv. Biotechnol. Exp. Ther. 2, 87-97.
Ivanov, A.V., Valuev-Elliston, V.T., Ivanova, O.N., Kochetkov, S.N., Starodubova, E.S., Bartosch, B., Isaguliants, M.G., 2016. Oxidative stress during HIV infection: Mechanisms and consequences. Oxid. Med. Cell. Longev. 2016, 8910396.
Jones, M.P., 2015. Avian hematology. Vet. Clin. North. Am. Exot. Anim. Pract. 18, 51-61.
Kidd, P.M., 1997. Glutathione: systemic protectant against oxidative and free radical damage. Altern. Med. Rev. 2, 155-176.
Lopes, P.D, Freitas Neto, O.C., Batista, D.F.A., Denadai, J., Alarcon, M.F.F., Almeida, A.M., Vasconcelos, R.O., Setta, A., Barrow, P.A., Berchieri Junior, A., 2016. Experimental infection of chickens by a flagellated motile strain of Salmonella enterica serovar Gallinarum biovar Gallinarum. Vet. J. 214, 40-46.
Mdegela, R.H., Msoffe, P.L.M., Waihenya, R.W., Kasanga, J.C., Mtambo, M.M.A., Minga, U.M., Olsen, J.E., 2002. Comparative pathogenesis of experimental infections with Salmonella Gallinarum in local and commercial chickens. Trop. Anim. Health Prod. 34(3), 194-204.
Molbak, K., Gerner-Smit, P., Wegener, H.C., 2002. Increasing quinolones resistance in Salmonella enterica serotype Enteritidis. Emerg. Infect. Dis. 8, 524-525.
OIE, 2019. Fowl typhoid and pullorum disease. Available online: https://www.woah.org/
fileadmin/Home/eng/Health_standards/tahc/2018/en_chapitre_fowl_typhoid_pullorum_disease.htm.
Okafor, S.C, Ihedioha, J.I., Ezema, W.S., 2023. Hematological alterations in laying hens infected with Salmonella Gallinarum, and their relationship to egg production. J. Vet. Appl. Sci. 13(1), 109-117.
Okafor, S.C., Ihedioha, J.I., Ezema, W.S., Onyema, I., Ezema, A.S., Chah, K.F., 2024. Evaluation of the effects of experimental Salmonella Gallinarum infection on the hematology and oxidative stress markers in young pullets. Anim. Res. Int. 21(1), 5378-5388.
Okwori, A.E.J., Ogbe, R., Chollom, S.C., Agada, G.O.A., Ujah, A., Okwori, E., Adeyanju, O.N., Echeonwu, G.O.N., 2013. Isolation of Salmonella Gallinarum from poultry droppings in Jos metropolis, Plateau State. Nig. J. Agric. Vet. Sci. 5(2), 14-44.
Parvej, M.S., Nazir, K.H., Rahman, M.B., Jahan, M., Khan, M.F., Rahman, M., 2016. Prevalence and characterization of multi-drug resistant Salmonella Enterica serovar Gallinarum biovar Pullorum and Gallinarum from chicken. Vet. World. 9, 65-70.
Patterson, R.A., Leacke, D.S., 1998. Human serum cysteine and histidine inhibit the oxidation of low-density lipoprotein less at acidic pH. Fed. Euro. Biochem. Soc. Lett. 434, 317-321.
Prasanna, K., Paliwal, O.P., 2002. Experimental fowl typhoid and pullorum disease in chickens: clinical and pathomorphological studies. Indian J. Vet. Pathol. 26, 528-531.
Seo, K.W., Kim, J.J., Mo, I.P., Lee, Y.J., 2019. Molecular characteristics of antimicrobial resistance of Salmonella Gallinarum isolates from chickens in Korea, 2014 to 2018. Poult. Sci. 98, 5416-5423.
Shah, S.N., Kamil, S.A., Darzi, M.M., Mir, M.S., Bhat, S.A., 2013. Hematological and some biochemical changes in experimental fowl typhoid infection in broiler chickens. Comp. Clin. Pathol. 22, 83-91.
Simsek, S., Yuce, A., Utuk, A.E., 2006. Determination of serum malondialdehyde levels in sheep naturally infected with Dicrocoelium dendriticum. Firat Univ. Saglik. Bil. Dergisi. 20, 217-220.
Taiwo, V.O., Olaniyi, M.O., Ogunsanmi, A.O., 2003. Comparative plasma biochemical changes and susceptibility of erythrocytes to in vitro peroxidation during experimental Trypanosoma congolense and Trypanosoma brucei infection in sheep. Isreali. J. Vet. Med. 58(4), 112-117.
Thrall, M.A., Weiser, M.G., 2002. Hematology. In: Hendrix, C.M. (Ed.), Laboratory procedures for veterinary technicians, (4th edition), Mosby, Missouri, pp. 29-74.
Weydert, C.J., Cullen, J.J., 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat. Protoc. 5, 51-66.
Yasmin, S., Nawaz, M., Anjum, A.A., Ashraf, K., Ullah, N., Mustapha, A., Ali, M.A., Mehmood, A., 2019. Antibiotic susceptibility pattern of Salmonellae isolated from different districts of Punjab, Pakistan. Pak. Vet. J. 40, 98-102.
Zanetti, N.S., De Carli, S., Sonza, M.N., Lehmann, F.K.M., Kipper, D., Dias, K.K.R., Fonseca, A.S.K., Lunge, V.R., Ikuta, N., 2019. Molecular detection and characterization of Salmonella Gallinarum from poultry farms in Brazil. J. Appld. Poult. Res. 28, 1335-1341.
Zhou, X., Kang, X., Zhou, K., Yue, M., 2022. A global dataset for prevalence of Salmonella Gallinarum between 1945 and 2021. Sci. Data. 9(1), 495.