Simultaneous Use of Iron/Anticoccidial Treatment and Vaccination against Oedema Disease: Impact on the Development of Serum-Neutralising Antibodies, Hematinic and Anticoccidial Activities in Piglets
Abstract
:1. Introduction
2. Materials and Methods
2.1. General Husbandry and Management of Animals
2.2. Products
2.3. Experimental Design, Blinding, and Treatments
2.4. Serum Neutralisation Test
2.5. Hematinic Parameters and Parasitology Examination
2.6. Performance Evaluation
2.7. Statistics
3. Results
3.1. Serum Neutralisation
3.2. Haematinic Indices
3.3. Evaluation of Presence of C. suis Oocysts
3.4. Growth Performance
3.5. Mortality
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fairbrother, J.M.; Nadeau, E. Collibacillosis. In Diseases of Swine, 11th ed.; Zimmerman, J., Karriker, L.A., Ramirez, A., Schwartz, K.J., Stevenson, G.W., Zhang, J., Eds.; Wiley-Blackwell: Hoboken, NJ, USA, 2019; pp. 807–834. [Google Scholar]
- Kausche, F.M.; Dean, E.A.; Arp, L.H.; Samuel, J.E.; Moon, H.W. An experimental model for subclinical edema disease (Escherichia coli enterotoxemia) manifest as vascular necrosis in pigs. Am. J. Vet. Res. 1992, 53, 281–287. [Google Scholar] [CrossRef]
- Berger, P.I.; Hermanns, S.; Kerner, K.; Schmelz, F.; Bauerfeind, R.; Schüler, V.; Ewers, C.; Doherr, M.G. Cross-sectional study: Prevalence of oedema disease Escherichia coli (EDEC) in weaned piglets in Germany at pen and farm levels. Porc. Health Manag. 2023, 9, 49. [Google Scholar] [CrossRef] [PubMed]
- Fricke, R.; Bastert, O.; Gotter, V.; Brons, N.; Kamp, J.; Selbitz, H.J. Implementation of a vaccine against Shigatoxin 2e in a piglet producing farm with problems of Oedema disease: Case study. Porc. Health Manag. 2015, 1, 6. [Google Scholar] [CrossRef] [PubMed]
- Lillie-Jaschniski, K.; Köchling, M.; Lindner, T. Erste Erfahrungen mit dem Einsatz von ECOPORC SHIGA, der neuen Vakzine gegen die Ödemkrankheit-Auswertungen aus Feldversuchen in Deuschland. Tierärztl. Umschau. 2013, 68, 377–382. [Google Scholar]
- Bednorz, C.; Oelgeschläger, K.; Kinnemann, B.; Hartmann, S.; Neumann, K.; Pieper, R.; Bethe, A.; Semmler, T.; Tedin, K.; Schierack, P.; et al. The broader context of antibiotic resistance: Zinc feed supplementation of piglets increases the proportion of multi-resistant Escherichia coli in vivo. Int. J. Med. Microbiol. 2013, 303, 396–403. [Google Scholar] [CrossRef]
- Mesonero-Escuredo, S.; Morales, J.; Mainar-Jaime, R.C.; Díaz, G.; Arnal, J.L.; Casanovas, C.; Barrabés, S.; Segal, J. Effect of Edema Disease Vaccination on Mortality and Growth Parameters in Nursery Pigs in a Shiga Toxin 2e Positive Commercial Farm. Vaccines 2021, 9, 567. [Google Scholar] [CrossRef] [PubMed]
- Sperling, D.; Isaka, N.; Karembe, H.; Vanhara, J.; Vinduska, J.; Strakova, N.; Kalova, A.; Kolackova, I.; Karpiskova, R. Effect of the vaccination against Shiga toxin 2e in a farm with history of oedema disease, caused by atypical Escherichia coli producing Shiga toxin (STEC). Vet. Med.-Czech. 2022, 67, 510–518. [Google Scholar] [CrossRef]
- Bastert, O.; Fricke, R.; Sudendey, C.; Gnielka, D.; Luder, O. Effect of vaccination with ECOPORC SHIGA on overall mortality and use of antimicrobial medication due to edema disease (ED). In Proceedings of the 5th European Symposium of Porcine Health Management (ESPHM), Edinburgh, UK, 22–24 May 2013; p. 202. [Google Scholar]
- Lee, S.I.; Ntakiyisumba, E.; Won, G. Systematic review and network meta-analysis to compare vaccine effectiveness against porcine edema disease caused by Shiga toxin-producing Escherichia coli. Sci. Rep. 2022, 12, 6460. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Lipinski, P.; Starzyński, R.R.; Canonne-Hergaux, F.; Tudek, B.; Oliński, R.; Kowalczyk, P.; Dziaman, T.; Thibaudeau, O.; Gralak, M.A.; Smuda, E.; et al. Benefits and risks of iron supplementation in anemic neonatal pigs. Am. J. Pathol. 2010, 177, 1233–1243. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Dong, Z.; Wan, D.; Yang, H.; Li, G.; Zhang, Y.; Zhou, X.; Wu, X.; Yin, Y. Effects of Iron Deficiency on Serum Metabolome, Hepatic Histology, and Function in Neonatal Piglets. Animals 2020, 10, 1353. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Li, Y.; Hansen, S.L.; Borst, L.B.; Spears, J.W.; Moeser, A.J. Dietary Iron Deficiency and Over supplementation Increase Intestinal Permeability, Ion Transport, and Inflammation in Pigs. J. Nutr. 2016, 146, 1499–1505. [Google Scholar] [CrossRef]
- Knight, L.; Dilger, R.N. Longitudinal Effects of Iron Deficiency Anemia and Subsequent Repletion on Blood Parameters and the Rate and Composition of Growth in Pigs. Nutrients 2018, 10, 632. [Google Scholar] [CrossRef] [PubMed]
- Hinney, B.; Cvetkovic, V.; Espigares, D.; Vanhara, J.; Waehner, C.; Ruttkowski, B.; Selista, R.; Sperling, D.; Joachim, A. Cystoisospora suis control in Europe is not allways effective. Front. Vet. Sci. 2020, 7, 113. [Google Scholar] [CrossRef] [PubMed]
- Joachim, A.; Schwarz, L. Coccidia in Swine: Eimeria Species, Cystoisospora (sin. Isospora) suis. In Encyclopedia of Parasitology; Springer: Heidelberg/Berlin, Germany, 2015; pp. 1–5. [Google Scholar]
- Noonan, G.; Rand, J.; Priest, J.; Ainscow, J.; Blackshaw, J. Behavioural observations of piglets undergoing tail docking, teeth clipping and ear notching. Appl. Anim. Behav. 1994, 39, 203–213. [Google Scholar] [CrossRef]
- Marchant-Forde, J.N.; Lay, D.C., Jr.; McMunn, K.A.; Cheng, H.W.; Pajor, E.A.; Marchant-Forde, R.M. Postnatal piglet husbandry practices and well-being: The effects of alternative techniques delivered in combination. J. Anim. Sci. 2014, 92, 1150–1160. [Google Scholar] [CrossRef] [PubMed]
- Stoffel, N.U.; Drakesmith, H. Effects of iron status on adaptive immunity and vaccine efficacy: A review. Adv. Nutr. 2024, 8, 100238. [Google Scholar] [CrossRef] [PubMed]
- Savy, M.; Edmond, K.; Fine, P.E.; Hall, A.; Hennig, B.J.; Moore, S.E.; Prentice, A.M.; Mulholland, K.; Schaible, U.; Prentice, A.M. Landscape analysis of interactions between nutrition and vaccine responses in children. J. Nutr. 2009, 139, 2154S–2218S. [Google Scholar] [CrossRef]
- Stoffel, N.U.; Uyoga, M.A.; Mutuku, F.M.; Frost, J.N.; Mwasi, E.; Paganini, D.; Zimmermann, M.B.; van der Klis, F.R.M.; Malhotra, I.J.; Desiráe LaBeaud, A.; et al. Iron deficiency anemia at time of vaccination predicts decreased vaccine response and iron supplementation at time of vaccination increases humoral vaccine response: A birth cohort study and a randomized trial follow-up study in Kenyan infants. Front. Immunol. 2020, 11, 1313. [Google Scholar] [CrossRef]
- Jiang, Y.; Li, C.; Wu, Q.; An, P.; Huang, L.; Wang, J.; Chen, C.; Chen, X.; Zhang, F.; Zhang, X.; et al. Iron-dependent histone 3 lysine 9 demethylation controls B cell proliferation and humoral immune responses. Nat. Commun. 2019, 10, 2935. [Google Scholar] [CrossRef]
- Plotkin, S.A.; Gilbert, P.B. Nomenclature for immune correlates of protection after vaccination. Clin. Infect. Dis. 2012, 54, 1615–1617. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Sperling, D.; Freudenschuss, B.; Shrestha, A.; Hinney, B.; Karembe, H.; Joachim, A. Comparative efficacy of two parenteral iron-containing preparations, iron gleptoferron and iron dextran, for the prevention of anaemia in suckling piglets. Vet. Rec. Open 2018, 5, e000317. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- European Medicines Agency. CVMP Assessment Report for Forceris (EMEA/V/C/004329/0000). 2019. Available online: https://medicines.health.europa.eu/veterinary/en/documents/download/3b5c3354-7761-435c-aeb0-f31c5abc73fe (accessed on 21 February 2019).
- Pirro, F.; Wieler, L.H.; Failing, K.; Bauerfeind, R.; Baljer, G. Neutralizing antibodies against Shiga-like toxins from Escherichia coli in colostra and sera of cattle. Vet. Microbiol. 1995, 43, 131–141. [Google Scholar] [CrossRef] [PubMed]
- Bhattarai, S.; Nielsen, J.P. Early indicators of iron deficiency in large piglets at weaning. J. Swine Health Prod. 2015, 23, 10–17. [Google Scholar] [CrossRef]
- Joachim, A.; Ruttkowski, B.; Sperling, D. Detection of Cystoisospora suis in faeces of suckling piglets—When and how? A comparison of methods. Porcine Health Manag. 2018, 19, 20. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Linggood, M.A.; Thompson, J.M. Verotoxin production among porcine strains of Escherichia coli and its association with oedema disease. J. Med. Microbiol. 1987, 24, 359–362. [Google Scholar] [CrossRef] [PubMed]
- Skinner, C.; Patfield, S.; Stanker, L.H.; Fratamico, P.; He, X. New high-affinity monoclonal antibodies against Shiga toxin 1 facilitate the detection of hybrid Stx1/Stx2 in vivo. PLoS ONE 2014, 9, e99854. [Google Scholar] [CrossRef] [PubMed]
- Bielaszewska, M.; Idelevich, E.A.; Zhang, W.; Bauwens, A.; Schaumburg, F.; Mellmann, A.; Peters, G.; Karch, H. Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain. Antimicrob. Agents Chemother. 2012, 56, 3277–3282. [Google Scholar] [CrossRef] [PubMed]
- Schmid, S.M.; Steinhoff-Wagner, J. Impact of Routine Management Procedures on the Welfare of Suckling Piglets. Vet. Sci. 2022, 9, 32. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Karmali, M.A.; Mascarenhas, M.; Petric, M.; Dutil, L.; Rahn, K.; Ludwig, K.; Arbus, G.S.; Michel, P.; Sherman, P.M.; Wilson, J.; et al. Age-specific frequencies of antibodies to Escherichia coli verocytotoxins (Shiga toxins) 1 and 2 among urban and rural populations in southern Ontario. J. Infect. Dis. 2003, 14, 1724–1729. [Google Scholar] [CrossRef]
- Reymond, D.; Karmali, M.A.; Clarke, I.; Winkler, M.; Petric, M. Comparison of the western blot assay with the neutralizing-antibody and enzyme-linked immunosorbent assays for measuring antibody to verocytotoxin 1. J. Clin. Microbiol. 1997, 14, 609–613. [Google Scholar] [CrossRef]
- Gordon, V.M.; Whipp, S.C.; Moon, H.W.; O’Brien, A.D.; Samuel, J.E. An enzymatic mutant of Shiga-like toxin II variant is a vaccine candidate for edema disease of swine. Infect. Immun. 1992, 60, 485–490. [Google Scholar] [CrossRef] [PubMed]
- Kerner, K.; Bridger, P.S.; Köpf, G.; Fröhlich, J.; Barth, S.; Willems, H.; Bauerfeind, R.; Baljer, G.; Menge, C. Evaluation of biological safety in vitro and immunogenicity in vivo of recombinant Escherichia coli Shiga toxoids as candidate vaccines in cattle. Vet. Res. 2015, 46, 38. [Google Scholar] [CrossRef] [PubMed]
- Dular, U. Comparative studies of the in vivo toxin neutralization and the in vitro Vero cell assay methods for use in potency testing of diphtheria component in combined vaccines/toxoids. 1: Standardization of a modified Vero cell assay for toxin-antitoxin titration of immunized guinea-pig sera. Biologicals 1993, 21, 53–59. [Google Scholar] [CrossRef] [PubMed]
- CVMP Assessment Report for ECOPORC SHIGA (EMEA/V/C/002588/0000), EMA/CVMP/2235/2013. Available online: https://medicines.health.europa.eu/veterinary/en/documents/download/9a3f471e-f3c8-4c9b-8e1a-e527eaee6cc3 (accessed on 7 February 2013).
- Augustyniak, A.; Pomorska-Mól, M. Vaccination Failures in Pigs—The Impact of Chosen Factors on the Immunisation Efficacy. Vaccines 2023, 11, 230. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Greif, G. Immunity to coccidiosis after treatment with toltrazuril. Parasitol. Res. 2000, 86, 787–790. [Google Scholar] [CrossRef]
- Zimmermann, M.; Stoffel, N.; Uyoga, M.; Karanja, S. Effects of Anaemia and Iron Supplementation on Vaccine Response: A Birth Cohort Study and a Randomized Trial Follow-Up Study in Kenyan Infants. Curr. Dev. Nutr. 2020, 4 (Suppl. S2), nzaa054_187. [Google Scholar] [CrossRef]
- Svoboda, M.; Vaňhara, J.; Berlinská, J. Parenteral iron administration in suckling piglets—A review. Acta Vet. Brno 2017, 86, 249–261. [Google Scholar] [CrossRef]
- Ježek, J.; Starič, J.; Nemec, M.; Plut, J.; Oven, I.G.; Klinkon, M.; Štukelj, M. The influence of age, farm and physiological status on pig hematological profiles. J. Swine Health Prod. 2018, 26, 72–78. [Google Scholar]
- Martínez-Miró, S.; Tecles, F.; Ramón, M.; Escribano, D.; Hernández, F.; Madrid, J.; Orengo, J.; Martínez-Subiela, S.; Manteca, X.; Cerón, J.J. Causes, consequences and biomarkers of stress in swine: An update. BMC Vet. Res. 2016, 12, 171. [Google Scholar] [CrossRef]
Treatment | Detectable Neutralising Antibodies (≥0) (%) | Detectable Neutralising Antibodies (≥15) (%) | |
---|---|---|---|
Day 28 | T1—Different days | 87.88 b | 69.70 b |
T2—Simultaneously | 83.33 b | 63.69 b | |
Day 60 | T1—Different days | 96.97 a | 90.91 a |
T2—Simultaneously | 97.22 a | 91.67 a | |
P treatment | 0.6549 | 0.7161 | |
P time | 0.0157 | 0.0004 | |
P treatment × time | 0.0983 | 0.0047 |
Treatment | Buffer Zone (%) | Optimal (%) |
---|---|---|
Day 28 | ||
T1—Different days | 0.00 | 100.00 |
T2—Simultaneously | 5.56 | 94.44 |
Day 60 | ||
T1—Different days | 30.30 | 69.70 |
T2—Simultaneously | 36.11 | 63.89 |
P treatment × time | <0.0001 |
Treatment | Haemoglobin (g/dL) | Haematocrit (%) |
---|---|---|
Day 28 | ||
T1—Different days | 13.18 a | 40.21 a |
T2—Simultaneously | 11.44 b | 39.45 a |
Day 60 | ||
T1—Different days | 12.84 c | 36.30 b |
T2—Simultaneously | 11.15 c | 35.32 b |
SEM | 0.203 | 0.548 |
P treatment | 0.0274 | 0.0792 |
P time | <0.0001 | <0.0001 |
P treatment × time | 0.8324 | 0.8199 |
Body Weight (kg) | ADG (g/Day) | |||||
---|---|---|---|---|---|---|
Treatment | Day 0 | Day 21 | Day 60 | 0–21 Days | 21–60 Days | 0–60 Days |
T1—Different days | 1.85 | 7.14 | 18.93 | 293.9 | 311.4 | 305.1 |
T2—Simultaneously | 1.84 | 7.27 | 19.98 | 301.4 | 334 | 323.9 |
SEM | 0.077 | 0.244 | 0.608 | 13.51 | 14.69 | 10.86 |
p-value | 0.9731 | 0.4520 | 0.1061 | 0.3121 | 0.1495 | 0.1051 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Sperling, D.; Rodríguez, M.; Guerra, N.; Karembe, H.; Diesing, A.-K.; Manso, A.; de Frutos, L.; Morales, J. Simultaneous Use of Iron/Anticoccidial Treatment and Vaccination against Oedema Disease: Impact on the Development of Serum-Neutralising Antibodies, Hematinic and Anticoccidial Activities in Piglets. Vaccines 2024, 12, 1004. https://doi.org/10.3390/vaccines12091004
Sperling D, Rodríguez M, Guerra N, Karembe H, Diesing A-K, Manso A, de Frutos L, Morales J. Simultaneous Use of Iron/Anticoccidial Treatment and Vaccination against Oedema Disease: Impact on the Development of Serum-Neutralising Antibodies, Hematinic and Anticoccidial Activities in Piglets. Vaccines. 2024; 12(9):1004. https://doi.org/10.3390/vaccines12091004
Chicago/Turabian StyleSperling, Daniel, María Rodríguez, Nicolás Guerra, Hamadi Karembe, Anne-Kathrin Diesing, Alberto Manso, Laura de Frutos, and Joaquín Morales. 2024. "Simultaneous Use of Iron/Anticoccidial Treatment and Vaccination against Oedema Disease: Impact on the Development of Serum-Neutralising Antibodies, Hematinic and Anticoccidial Activities in Piglets" Vaccines 12, no. 9: 1004. https://doi.org/10.3390/vaccines12091004