Boric Acid in Milk Replacer as a Health Enhancer and Growth Promoter for Lambs in the Suckling Period.

Boric acid Gene expressions Immune system Lamb health Suckling period

Journal

Biological trace element research
ISSN: 1559-0720
Titre abrégé: Biol Trace Elem Res
Pays: United States
ID NLM: 7911509

Informations de publication

Date de publication:
17 May 2024
Historique:
received: 26 03 2024
accepted: 27 04 2024
medline: 17 5 2024
pubmed: 17 5 2024
entrez: 17 5 2024
Statut: aheadofprint

Résumé

This study was performed to investigate the effects of boric acid supplementation in milk replacer of lambs in the suckling period on performance, biochemical parameters, the antioxidant system, fecal culture, and expression of some genes. During the suckling period, 60 lambs (4 days old) were randomly given four levels of boric acid (0, 30, 60, and 90 mg/kg body weight) via milk replacer for 57 days. The lambs supplemented with boric acid had a higher weight gain and better feed conversion ratio. Boric acid supplementation quadratically increased serum triglyceride, total protein, alkaline phosphatase, serum antioxidant activity and oxidative stress biomarkers, and fecal flora and decreased IL1β, IL10, iNOS, NF-kB, and TNF-α gene expressions. The effect of boric acid on rumen papilla development could not be determined since the animals were not slaughtered. In conclusion, the use of boric acid to lambs in the suckling period improved the average weekly body weight gain and feed conversion efficiency, positively affected some biochemical parameters, antioxidant system, and intestinal flora, and also affected gene expressions related to the immune system. Boric acid supplementation had a beneficial effect on the health and growth of suckling lambs.

Identifiants

pubmed: 38758480
doi: 10.1007/s12011-024-04214-4
pii: 10.1007/s12011-024-04214-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Scientific Research Projects Fund of Ataturk University
ID : TDK-2021-9092

Informations de copyright

© 2024. The Author(s).

Références

Henchion M, Moloney AP, Hyland J, Zimmermann J, McCarthy S (2021) Trends for meat, milk and egg consumption for the next decades and the role played by livestock systems in the global production of proteins. Animal 15:100287. https://doi.org/10.1016/j.animal.2021.100287
doi: 10.1016/j.animal.2021.100287 pubmed: 34312092
Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. https://doi.org/10.22004/ag.econ.288998
Xia Q, Wang X, Pan Z, Zhang R, Wei C, Chu M, Di R (2021) Genetic diversity and phylogenetic relationship of nine sheep populations based on microsatellite markers. Arch Animal Breed 64(1):7–16. https://doi.org/10.5194/aab-64-7-2021
doi: 10.5194/aab-64-7-2021
Besufkad S, Abebe A, Getachew T, Goshme S, Bisrat A, Abebe A, Gizaw S (2024) Survival analysis of genetic and non-genetic factors influencing lamb survival of different sheep breeds. Small Rumin Res 232:107206. https://doi.org/10.1016/j.smallrumres.2024.107206
doi: 10.1016/j.smallrumres.2024.107206
Johnson T, Jacobson BT, Jones K, Mosdal C, Jones S, Vitkovic M, Bimczok D (2022) Transfer and persistence of bovine immunoglobulins in lambs fed a colostrum replacer. Vet Record 191(10):1–5. https://doi.org/10.1002/vetr.1974
doi: 10.1002/vetr.1974
Bagath M, Krishnan G, Devaraj C, Rashamol VP, Pragna P, Lees AM, Sejian V (2019) The impact of heat stress on the immune system in dairy cattle: a review. Res Vet Sci 126:94–102
doi: 10.1016/j.rvsc.2019.08.011 pubmed: 31445399
Arshad MA, Hassan FU, Rehman MS, Huws SA, Cheng Y, Din AU (2021) Gut microbiome colonization and development in neonatal ruminants: strategies, prospects, and opportunities. Animal Nutr 7(3):883–895. https://doi.org/10.1016/j.aninu.2021.03.004
doi: 10.1016/j.aninu.2021.03.004
Fu L, Wang L, Liu L, Zhang L, Zhou Z, Zhou Y, Dong X (2023) Effects of inoculation with active microorganisms derived from adult goats on growth performance, gut microbiota and serum metabolome in newborn lambs. Front Microbiol 14:1128271. https://doi.org/10.3389/fmicb.2023.1128271
doi: 10.3389/fmicb.2023.1128271 pubmed: 36860489 pmcid: 9969556
Hunter JM, Nemzer BV, Rangavajla N, Biţă A, Rogoveanu OC, Neamţu J, Mogoşanu GD (2019) The fructoborates: part of a family of naturally occurring sugar–borate complexes—biochemistry, physiology, and impact on human health: a review. Biol Trace Elem Res 188:11–25
doi: 10.1007/s12011-018-1550-4 pubmed: 30343480
Zhu Y, Cai J, Hosmane NS, Zhang Y (2022) Introduction: basic concept of boron and its physical and chemical properties. Fundamentals Appl Boron Chem 2:1–57. https://doi.org/10.1016/B978-0-12-822127-3.00003-X
doi: 10.1016/B978-0-12-822127-3.00003-X
Khaliq H, Juming Z, Ke-Mei P (2018) The physiological role of boron on health. Biol Trace Elem Res 186:31–51
doi: 10.1007/s12011-018-1284-3 pubmed: 29546541
Matthes MS, Robil JM, McSteen P (2020) From element to development: the power of the essential micronutrient boron to shape morphological processes in plants. J Exp Bot 71(5):1681–1693
doi: 10.1093/jxb/eraa042 pubmed: 31985801 pmcid: 7067301
Sharma A, Man V, Pal RP, Sarkar S, Datt C (2020) Boron supplementation in peripartum Murrah buffaloes: the effect on calcium homeostasis, bone metabolism, endocrine and antioxidant status. J Trace Elem Med Biol 62:126623. https://doi.org/10.1016/j.jtemb.2020.126623
doi: 10.1016/j.jtemb.2020.126623 pubmed: 32739828
Kar F, Hacioglu C, Senturk H, Donmez DB, Kanbak G (2020) The role of oxidative stress, renal inflammation, and apoptosis in post ischemic reperfusion injury of kidney tissue: the protective effect of dose-dependent boric acid administration. Biol Trace Elem Res 195(1):150–158. https://doi.org/10.1007/s12011-019-01824-1
doi: 10.1007/s12011-019-01824-1 pubmed: 31372827
Türkez H, Geyikoǧlu F, Tatar A, Keleş S, Özkan A (2007) Effects of some boron compounds on peripheral human blood. Zeitschrift Fur Naturforschung - Section C J Biosci 62(11–12):889–896. https://doi.org/10.1515/znc-2007-11-1218
doi: 10.1515/znc-2007-11-1218
Borokhov O, Schubert D (2007) Antimicrobial properties of boron derivatives. ACS Symp Ser 967:412–435. https://doi.org/10.1021/bk-2007-0967.ch020
doi: 10.1021/bk-2007-0967.ch020
Bozkurt M, Küçükyilmaz K, Çath AU, Çinar M, Çabuk M, Bintaş E (2012) Effects of boron supplementation to diets deficient in calcium and phosphorus on performance with some serum, bone and fecal characteristics of broiler chickens. Asian Australas J Anim Sci 25(2):248–255. https://doi.org/10.5713/ajas.2011.11211
doi: 10.5713/ajas.2011.11211 pubmed: 25049558 pmcid: 4093127
Kabu M, Civelek T, Birdane FM (2014) Effects of boron, propylene glycol and methionine administration on some hematological parameters in dairy cattle during periparturient period. Veterinarski arhiv 84(1):19–29
Sizmaz Ö, Yildiz G (2014) Effects of dietary boric acid and ascorbic acid supplementation on performance, some blood and bone parameters in broilers. Kafkas Universitesi Veteriner Fakultesi Dergisi 20(1):55–61. https://doi.org/10.9775/kvfd.2013.9451
doi: 10.9775/kvfd.2013.9451
Schmidt M (2017) Boric acid inhibition of Trichophyton rubrum growth and conidia formation. Biol Trace Elem Res 180(2):349–354. https://doi.org/10.1007/s12011-017-1019-x
doi: 10.1007/s12011-017-1019-x pubmed: 28391495
Bhasker TV, Gowda NKS, Mondal S, Krishnamoorthy P, Pal DT, Mor A, Bhat SK, Pattanaik AK (2016) Boron influences immune and antioxidant responses by modulating hepatic superoxide dismutase activity under calcium deficit abiotic stress in Wistar rats. J Trace Elem Med Biol 36:73–79. https://doi.org/10.1016/j.jtemb.2016.04.007
doi: 10.1016/j.jtemb.2016.04.007 pubmed: 27259355
Romero-Aguilar KS, Arciniega-Martínez IM, Farfán-García ED, Campos-Rodríguez R, Reséndiz-Albor AA, Soriano-Ursúa MA (2019) Effects of boron-containing compounds on immune responses: review and patenting trends. Expert Opin Ther Pat 29(5):339–351. https://doi.org/10.1080/13543776.2019.1612368
doi: 10.1080/13543776.2019.1612368 pubmed: 31064237
Gowda NKS, Gopi M, Pal DT, Dey DK, Bhasker TV (2023) Bioactive role of dietary boron in animals: a review. Anim Nutr Feed Technol 23(2):437–453. https://doi.org/10.5958/0974-181X.2023.00037.9
doi: 10.5958/0974-181X.2023.00037.9
Pizzorno L (2015) Nothing boring about boron. Integr Med: A Clin J 14(4):35
Singh AK, Kewalramani N, Mani V, Sharma A, Kumari P, Pal RP (2021) Effects of boric acid supplementation on bone health in crossbred calves under tropical condition. J Trace Elem Med Biol 63:126647. https://doi.org/10.1016/j.jtemb.2020.126647
doi: 10.1016/j.jtemb.2020.126647 pubmed: 33010650
Huang Y, Wang G, Li C, Wang W, Zhang X, Wang X, Ma Z (2022) Periodical changes of feces microbiota and its relationship with nutrient digestibility in early lambs. Animals 12(14):1770. https://doi.org/10.3390/ani12141770
doi: 10.3390/ani12141770 pubmed: 35883317 pmcid: 9311505
Placer ZA, Cushman LL, Johnson BC (1966) Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal Biochem 16(2):359–364. https://doi.org/10.1016/0003-2697(66)90167-9
doi: 10.1016/0003-2697(66)90167-9 pubmed: 6007581
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25(C):192–205. https://doi.org/10.1016/0003-2697(68)90092-4
doi: 10.1016/0003-2697(68)90092-4 pubmed: 4973948
Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38(12):1103–1111. https://doi.org/10.1016/j.clinbiochem.2005.08.008
doi: 10.1016/j.clinbiochem.2005.08.008 pubmed: 16214125
Erel O (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37(4):277–285. https://doi.org/10.1016/j.clinbiochem.2003.11.015
doi: 10.1016/j.clinbiochem.2003.11.015 pubmed: 15003729
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408
doi: 10.1006/meth.2001.1262 pubmed: 11846609
Piccione G, Borruso M, Fazio F, Giannetto C, Caola G (2007) Physiological parameters in lambs during the first 30 days postpartum. Small Rumin Res 72(1):57–60. https://doi.org/10.1016/j.smallrumres.2006.04.002
doi: 10.1016/j.smallrumres.2006.04.002
Angell J, Duncan J (2020) Watery mouth disease in neonatal lambs: a systematic literature review. Livestock 25(2):94–103. https://doi.org/10.12968/live.2020.25.2.94
doi: 10.12968/live.2020.25.2.94
Bhasker TV, Gowda NKS, Pal DT, Bhat SK, Krishnamoorthy P, Mondal S, Pattanaik AK, Verma AK (2017) Influence of boron supplementation on performance, immunity and antioxidant status of lambs fed diets with or without adequate level of calcium. PLoS ONE 12(11):1–14. https://doi.org/10.1371/journal.pone.0187203
doi: 10.1371/journal.pone.0187203
Jin E, Gu Y, Wang J, Jin G, Li S (2014) Effect of supplementation of drinking water with different levels of boron on performance and immune organ parameters of broilers. Ital J Anim Sci 13(2):3152
doi: 10.4081/ijas.2014.3152
Krishnan BB, Selvaraju S, Gowda NKS, Subramanya KB, Pal D, Archana SS, Bhatta R (2019) Dietary boron supplementation enhances sperm quality and immunity through influencing the associated biochemical parameters and modulating the genes expression at testicular tissue. J Trace Elem Med Biol 55:6–14. https://doi.org/10.1016/j.jtemb.2019.05.004
doi: 10.1016/j.jtemb.2019.05.004 pubmed: 31345367
Hakan KB, Gultekin Y, Ozge S (2012) Effects of boric acid and humate supplementation on performance and egg quality parameters of laying hens. Braz J Poultry Sci 14:283–289
doi: 10.1590/S1516-635X2012000400008
Ayasan T, Yurtseven S, Baylan M, Kutlu HR (2011) Effects of boric acid supplementation on egg production and quality of Japanese quails (Coturnix coturnix Japonica). Indian J Anim Sci 81(5):534
Cho HM, Macelline SP, Wickramasuriya SS, Shin TK, Kim E, Son HC, Heo JM (2022) Moderate dietary boron supplementation improved growth performance, crude protein digestibility and diarrhea index in weaner pigs regardless of the sanitary condition. Anim Biosci 35(3):434. https://doi.org/10.5713/ab.21.0110
doi: 10.5713/ab.21.0110 pubmed: 34293844
Oz M, Tatil T, Dikel S (2021) Effects of boric acid on the growth performance and nutritional content of rainbow trout (Oncorhynchus mykiss). Chemosphere 272:129895. https://doi.org/10.1016/j.chemosfer.2021.129895
doi: 10.1016/j.chemosfer.2021.129895 pubmed: 35534968
Öz M, Inanan BE, Dikel S (2018) Effect of boric acid in rainbow trout (Oncorhynchus mykiss) growth performance. J Appl Anim Res 46(1):990–993. https://doi.org/10.1080/09712119.2018.1450258
doi: 10.1080/09712119.2018.1450258
Basoglu A, Sevinc M, Birdane FM, Boydak M (2002) Efficacy of sodium borate in the prevention of fatty liver in dairy cows. J Vet Intern Med 16:732–735
doi: 10.1111/j.1939-1676.2002.tb02416.x pubmed: 12465773
Eren M, Uyanik F, Guclu BK, Atasever A (2012) The influence of dietary boron supplementation on performance, some biochemical parameters and organs in broilers. Asian J Anim Vet Adv 7(11):1079–1089. https://doi.org/10.3923/ajava.2012.1079.1089
doi: 10.3923/ajava.2012.1079.1089
Elkomy AE, Abd El-hady AM, Elghalid OA (2015) Dietary boron supplementation and its impact on semen characteristics and physiological status of adult male rabbits. Asian J Poultry Sci 9(2):85–96. https://doi.org/10.3923/ajpsaj.2015.85.96
doi: 10.3923/ajpsaj.2015.85.96
Teneva A, Hristov K, Stoimenov G (2020) Blood biochemical profiles of dairy cows and their calves from Bulgarian black and white cattle breed. Bulgarian J Agr Sci 26(4):890–893
Kabu M, Birdane FM, Civelek T, Uyarlar C (2013) Affects of boron administration on serum Ca, Mg and P of peripartum Cows. Arch Anim Breed 56(1):733–741. https://doi.org/10.7482/0003-9438-56-073
doi: 10.7482/0003-9438-56-073
Abdelnour SA, Abd El-Hack ME, Swelum AA, Perillo A, Losacco C (2018) The vital roles of boron in animal health and production: a comprehensive review. J Trace Elem Med Biol 50(June):296–304. https://doi.org/10.1016/j.jtemb.2018.07.018
doi: 10.1016/j.jtemb.2018.07.018 pubmed: 30262295
Ayşeşek N, Arısan V, Balcıoğlu NB, Erol A, Kuruoğlu F, Tekkeşin MS, Ersanlı S (2022) Boron- and boric acid-treated titanium implant surfaces in sheep tibia : a histologic, histomorphometric and mechanical study. Bioengineering 9(705):1–15
Bharti VK, Gupta M, Lall D, Kapoor V (2007) Effects of boron on haemogram and biochemical profile of urine in buffalo calves fed a high fluoride ration. Fluoride 40(4):238–243
Gökce E, Cihan P, Atakişi O, Kirmizigül AH, Erdoğan HM (2022) Oxidative stress in neonatal lambs and its relation to health status and passive colostral immunity. Vet Immunol Immunopathol 251:110470
doi: 10.1016/j.vetimm.2022.110470 pubmed: 35985179
Cikler-Dulger E, Sogut I (2020) Investigation of the protective effects of boric acid on ethanol induced kidney injury. Biotech Histochem 95(3):186–193. https://doi.org/10.1080/10520295.2019.1662086
doi: 10.1080/10520295.2019.1662086 pubmed: 32041435
Ince S, Kucukkurt I, Cigerci IH, Fatih Fidan A, Eryavuz A (2010) The effects of dietary boric acid and borax supplementation on lipid peroxidation, antioxidant activity, and DNA damage in rats. J Trace Elem Med Biol 24(3):161–164. https://doi.org/10.1016/j.jtemb.2010.01.003
doi: 10.1016/j.jtemb.2010.01.003 pubmed: 20569927
Hazman Ö, Bozkurt MF, Fidan AF, Uysal FE, Çelik S (2018) The effect of boric acid and borax on oxidative stress, inflammation, ER stress and apoptosis in cisplatin toxication and nephrotoxicity developing as a result of toxication. Inflammation 41(3):1032–1048. https://doi.org/10.1007/s10753-018-0756-0
doi: 10.1007/s10753-018-0756-0 pubmed: 29500724
Yazc S, Akşit H, Korkut O, Sunay B, Çelik T (2014) Effects of boric acid and 2-aminoethoxydiphenyl borate on necrotizing enterocolitis. J Pediatr Gastroenterol Nutr 58(1):61–67. https://doi.org/10.1097/MPG.0b013e3182a7e02b
doi: 10.1097/MPG.0b013e3182a7e02b
Korkmaz M, Turkmen R, Demirel HH, Saritas ZK (2019) Effect of boron on the repair of osteochondral defect and oxidative stress in rats: an experimental study. Biol Trace Elem Res 187(2):425–433. https://doi.org/10.1007/s12011-018-1381-3
doi: 10.1007/s12011-018-1381-3 pubmed: 29869015
Wang Y, Zhang H, LinZhu LZ, Xu Y, Liu N, Sun X, Hu L, Huang H, Wei K, Zhu R (2018) Dynamic distribution of gut microbiota in goats at different ages and health states. Front Microbiol 9(OCT):1–10. https://doi.org/10.3389/fmicb.2018.02509
doi: 10.3389/fmicb.2018.02509
Smith B, Bodé S, Petersen BL, Jensen TK, Pipper C, Kloppenborg J, Boyé M, Krogfelt KA, Mølbak L (2011) Community analysis of bacteria colonizing intestinal tissue of neonates with necrotizing enterocolitis. BMC Microbiol 11. https://doi.org/10.1186/1471-2180-11-73
Kong LC, Wang B, Wang YM, Hu RG, Atiewin A, Gao D, Ma HX (2019) Characterization of bacterial community changes and antibiotic resistance genes in lamb manure of different incidence. Sci Rep 9(1):10101. https://doi.org/10.1038/s41598-019-46604-y
doi: 10.1038/s41598-019-46604-y pubmed: 31300748 pmcid: 6625992
Sun J, Chen W, Yuan Z (2022) Characterization of intestinal microbiota in lambs with different susceptibility to Escherichia coli F17. Vet Sci 9(12):670
doi: 10.3390/vetsci9120670 pubmed: 36548832 pmcid: 9782581
Bi Y, Cox MS, Zhang F, Suen G, Zhang N, Tu Y, Diao Q (2019) Feeding modes shape the acquisition and structure of the initial gut microbiota in newborn lambs. Environ Microbiol 21(7):2333–2346. https://doi.org/10.1111/1462-2920.14614
doi: 10.1111/1462-2920.14614 pubmed: 30938032 pmcid: 6849743
Uzal FA, Giannitti F, Asin J (2022) Yellow lamb disease (Clostridium perfringens type A enterotoxemia of sheep): a review. Animals 12(12):1–9. https://doi.org/10.3390/ani12121590
doi: 10.3390/ani12121590
Rafferty R, Robinson VH, Harris J, Argyle SA, Nuttall TJ (2019) A pilot study of the in vitro antimicrobial activity and in vivo residual activity of chlorhexidine and acetic acid/boric acid impregnated cleansing wipes. BMC Vet Res 15(1):382. https://doi.org/10.1186/s12917-019-2098-z
doi: 10.1186/s12917-019-2098-z pubmed: 31666075 pmcid: 6820967
Li J, Xu L, Sang R, Yu Y, Ge B, Zhang X (2018) Immunomodulatory and anti-inflammatory effects of total flavonoids of Astragalus by regulating NF-κB and MAPK signalling pathways in RAW 2647 macrophages. Pharmazie 73(10):589–593. https://doi.org/10.1691/ph.2018.8633
doi: 10.1691/ph.2018.8633 pubmed: 30223923
Çelik H, Kandemir FM, Caglayan C, Özdemir S, Çomaklı S, Kucukler S, Yardım A (2020) Neuroprotective effect of rutin against colistin-induced oxidative stress, inflammation and apoptosis in rat brain associated with the CREB/BDNF expressions. Mol Biol Rep 47:2023–2034. https://doi.org/10.1007/s11033-020-05302-z
doi: 10.1007/s11033-020-05302-z pubmed: 32030599
Wu YQ, Dang RL, Tang MM, Cai HL, Li HD, Liao DH, Jiang P (2016) Long chain omega-3 polyunsaturated fatty acid supplementation alleviates doxorubicin-induced depressive-like behaviors and neurotoxicity in rats: involvement of oxidative stress and neuroinflammation. Nutrients 8(4):243. https://doi.org/10.3390/nu8040243
doi: 10.3390/nu8040243 pubmed: 27120616 pmcid: 4848711
Routray I, Ali S (2016) Boron induces lymphocyte proliferation and modulates the priming effects of lipopolysaccharide on macrophages. PLoS ONE 11(3):1–17. https://doi.org/10.1371/journal.pone.0150607
doi: 10.1371/journal.pone.0150607
Fry RS, Brown TT, Lloyd KE, Hansen SL, Legleiter LR, Robarge WP, Spears JW (2011) Effect of dietary boron on physiological responses in growing steers inoculated with bovine herpesvirus type-1. Res Vet Sci 90(1):78–83. https://doi.org/10.1016/j.rvsc.2010.04.016
doi: 10.1016/j.rvsc.2010.04.016 pubmed: 20493506
Gul S, Cicek D, Sahin K, Ozercan IH, Orhan C, Demir B, Er B (2022) Effect of boron element on photoaging in rats. J Photochem Photobiol B: Biol 230(2021):112440. https://doi.org/10.1016/j.jphotobiol.2022.112440
doi: 10.1016/j.jphotobiol.2022.112440

Auteurs

Soner Uysal (S)

Department of Animal Nutrition and Nutritional Diseases, Faculty of Veterinary Medicine, Ataturk University, Erzurum, 25240, Turkey. soneruysal33@gmail.com.

Mehmet Akif Yoruk (MA)

Department of Animal Nutrition and Nutritional Diseases, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun, 55139, Turkey.

Classifications MeSH