Please wait a minute...
Journal of Integrative Agriculture  2026, Vol. 25 Issue (8): 3379-3386    DOI: 10.1016/j.jia.2024.08.025
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Maternal chromium supplementation improves oxidation resistance, immunity, and intestinal morphology of goat kids injected with lipopolysaccharide

Yujuan Li1, 2, Chengcheng Dai1, 2, Fang Xiao1, 2, Jerry W Spears3, Yanhua Gao1, 2, Fei Jiang1, 2, Haitao Shi1, 2, Yanling Huang1, 2#

1 Key Laboratory of Animal Science of State Ethnic Affairs Commission, Southwest Minzu University, Chengdu 610041, China

2 Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610041, China

3 Department of Animal Science, North Carolina State University, Raleigh, NC 27695-7621, USA

 Highlights 
Maternal chromium (Cr) supplementation can be transferred to offspring via both placenta and colostrum.
Maternal Cr supplementation increased serum immunoglobulin concentrations and antioxidant capacity of goat kids.
Maternal Cr supplementation improved the intestinal morphology of goat kids.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

本试验研究了母羊铬补充对子代脂多糖(lipopolysaccharide, LPS)应激羔羊抗氧化、免疫功能及肠道形态的影响。选取40只妊娠90天(90±3.53天)的乐至黑山羊,按体重(52.36±8.24 kg)随机分为4个处理,每组10个重复,每个重复1只母羊,单栏单饲。对照组饲喂基础日粮(实测铬含量为0.29 mg kg-1),铬补充组在饲喂基础日粮的基础上,每头母羊每日以丙酸铬(Cr propionate, CrPro)的形式补充0.41.22.0 mg的铬,直至子代羔羊21日龄。羔羊出生当日,采集母羊初乳和脐带样品,测定初乳中免疫球蛋白含量及初乳和脐带中铬含量。羔羊哺乳至21日龄,每重复选取一只雄性羔羊LPS注射2 h后采血、屠宰,测定羔羊血清及肝脏抗氧化指标、血清免疫球蛋白含量、肝脏铬含量及十二指肠、空肠、回肠肠道形态。结果表明:1)母羊铬补充对子代羔羊的初生重、窝重及21日龄体重、窝重无影响(P>0.05)。2)母羊初乳、脐带及子代羔羊肝脏铬含量随母羊铬补充量的提高线性增加(P<0.05)。3)随母羊铬补充量提高,子代羔羊血清总超氧化物歧化酶(Total Superoxide dismutase, T-SOD)活性呈二次曲线升高丙二醛(Malondialdehyde, MDA)含量线性降低,谷胱甘肽过氧化物酶(Glutathione peroxidase, GSH-Px活性线性升高(P<0.05)。4)随母羊铬补充量的增加,初乳中免疫球蛋白AImmunoglobulin A, IgA)、免疫球蛋白GImmunoglobulin G, IgG)和免疫球蛋白MImmunoglobulin M, IgM)含量线性增加;子代羔羊血清IgGIgM含量随母羊铬补充量的增加呈二次曲线增加,均在铬补充量为每头每日0.4 mg时达到最高(P<0.05)。5母羊铬补充量的增加,子代羔羊十二指肠绒毛高度(Villus height, VH)和绒毛高度/隐窝深度(Villus height to crypt depth ratio, V/C)呈二次曲线升高,且均在铬补充量为每头每日1.2 mg时达到最高;回肠隐窝深度(Crypt depth, CD)线性降低(P<0.05)。本试验范围内,每头母羊每日补充0.4-2.0 mg(实测值0.47-2.41 mg)来源于丙酸铬的铬可改善子代LPS应激羔羊抗氧化、免疫功能及肠道形态。本研究首次发现铬补充可提高母羊初乳免疫球蛋白含量及初乳和脐带铬沉积,并改善了子代LPS应激羔羊的抗氧化、免疫功能及肠道形态,研究结果为铬在妊娠动物中的应用提供了理论依据。



Abstract  

This study evaluated the effects of maternal chromium (Cr), supplemented with Cr propionate (CrPro) during perinatal period of does, on antioxidant capacity, immune response, and intestinal morphology of goat kids injected with lipopolysaccharide (LPS).  Forty Lezhi black does at 90 d of pregnancy were divided into 4 groups based on body weight (52.36±8.24) kg with 10 replicate pens for each treatment and one doe for each replicate pen.  Treatments consisted of 0, 0.4, 1.2, or 2.0 mg of supplemental Cr per head per day (per head d–1) from CrPro.  After birth, the goat kids were allowed to suckle until 21 d.  At 21-d-old, one male goat kid per replicate was sacrificed 2 h after LPS injection.  Individual weight and litter weight of goat kids at birth and 21 d were not affected by maternal Cr supplementation.  Chromium concentrations in umbilical cord, colostrum and liver of goat kids were linearly increased by maternal Cr supplementation (P<0.05).  Maternal Cr supplementation quadratically increased serum total superoxide dismutase (T-SOD) activity of goat kids (P<0.05).  Goat kids from maternal Cr supplementation groups had higher serum T-SOD activity than those from the control group (P<0.05).  Serum malondialdehyde (MDA) concentration of goat kids was linearly decreased, whereas serum glutathione peroxidase (GSH-Px) activity was linearly increased as maternal Cr increased (P<0.05).  Maternal Cr supplementation linearly increased colostrum immunoglobulin A (IgA), immunoglobulin G (IgG) and immunoglobulin M (IgM) concentrations (P<0.05), and quadratically increased serum IgG and IgM concentrations of goat kids with the greatest response detected at 0.4 mg
per head d–1 maternal Cr supplementation group (P<0.05).  The villus height (VH) and the ratio of VH to crypt depth (CD) (V/C) in the duodenum of goat kids increased quadratically as maternal Cr increased, and both reached the highest values in the 1.2 mg per head d–1 maternal Cr supplementation group.  Maternal Cr supplementation linearly decreased ileal CD of goat kids.  The results indicate that 0.4–2.0 mg (0.47–2.41 mg by analysis) per head d–1 maternal Cr supplementation from CrPro could improve antioxidant capacity, immune response, and small intestinal morphology of goat kids injected with LPS.  

Keywords:  maternal chromium supplementation       goat kids        antioxidant capacity        immune response        intestinal morphology  
Received: 12 June 2024   Accepted: 21 August 2024 Online: 27 August 2024  
Fund: This work was supported by the Sichuan Provincial Key R&D Project, China (22ZDYF0194), the Innovation Team Development Funds for Sichuan Beef, China (SCCXTD-2024-13), the Double World-Class Project of Southwest Minzu University, China (XM2023010), the Scientific and Technological Innovation Team Qinghai-Tibetan Plateau for Research in Southwest Minzu University, China (2024CXTD17).
About author:  Yujuan Li, E-mail: hbhsyj@163.com; #Correspondence Yanling Huang, Tel: +86-28-85522310, E-mail: swunylh@163.com

Cite this article: 

Yujuan Li, Chengcheng Dai, Fang Xiao, Jerry W Spears, Yanhua Gao, Fei Jiang, Haitao Shi, Yanling Huang. 2026. Maternal chromium supplementation improves oxidation resistance, immunity, and intestinal morphology of goat kids injected with lipopolysaccharide. Journal of Integrative Agriculture, 25(8): 3379-3386.

Abuelo A, Hernández J, Benedito J L, Castillo C. 2019. Redox biology in transition periods of dairy cattle: Role in the health of periparturient and neonatal animals. Antioxidants8, 20.

Anderson R A, Bryden N A, Polansky M M, Deuster P A. 1988. Exercise effects on chromium excretion of trained and untrained men consuming a constant diet. Journal of Applied Physiology64, 249–252.

AOAC (Association of Official Analytical Chemists). 1990. Official Methods of Analysis. 9th ed. Association of Official Analytical Chemists, Arlington, VA, USA.

Banse H E, Frank N, Kwong G P S, McFarlane D. 2015. Relationship of oxidative stress in skeletal muscle with obesity and obesity associated hyperinsulinemia in horses. Canadian Journal of Veterinary Research79, 329–338.

Bernhard B C, Burdick N C, Rounds W, Rathmann R J, Carroll J A, Finck D N, Jennings M A, Young T R, Johnson B J. 2012. Chromium supplementation alters the performance and health of feedlot cattle during the receiving period and enhances their metabolic response to a lipopolysaccharide challenge. Journal of Animal Science90, 3879–3888.

Brochine L, dos Santos F F, Moreira F M, de Zoppa A L, Leme P R, Tedeschi L O, Gallo S B. 2023. The impact of fetal programming in ewe nutrition with chromium propionate or calcium salts of palm oil on the meat quality and bone of the progeny. Biological Trace Element Research201, 2331–2340.

Burdick N C, Bernhard B C, Carroll J A, Rathmann R J, Johnson B J. 2012. Enhancement of the acute phase response to a lipopolysaccharide challenge in steers supplemented with chromium. Innate Immunity18, 592–601.

Cecerska-Heryć E, Polikowska A, Serwin N, Roszak M, Grygorcewicz B, Heryć R, Michalczyk A, Dołęgowska B. 2022. Importance of oxidative stress in the pathogenesis, diagnosis, and monitoring of patients with neuropsychiatric disorders, a review. Neurochemistry International153, 105269.

Charneca R, Vila-Viçosa J M, Infante P, Nunes J, Dividich L J. 2015. Colostrum production of Alentejano and Large-White×Landrace sows: Consumption, passive immunity and mortality of piglets. Spanish Journal of Agricultural Research13, e0611.

Chen J F, Xing Y, Nie M, Xu M M, Huang H F, Xie H, Liao J H, Lin X, Duan J N, Zhang J X. 2024. Comparative effects of various dietary selenium sources on growth performance, meat quality, essential trace elements content, and antioxidant capacity in broilers. Poultry Science103, 104057.

Chen X L, Zeng Y B, Liu L X, Song Q L, Zou Z H, Wei Q P, Song W J. 2021. Effects of dietary chromium propionate on laying performance, egg quality, serum biochemical parameters and antioxidant status of laying ducks under heat stress. Animal15, 100081.

Debata N R, Sethy K, Swain R K, Mishra S K, Panda N, Maity S. 2023. Supplementation of nano-selenium (SeNPs) improved growth, immunity, antioxidant enzyme activity, and selenium retention in broiler chicken during summer season. Tropical Animal Health and Production55, 260.

Du L Y, Lu J B, Cui Z J, He M Y. 2006. Effect of supplementation chromium on reproductive performance in multiparous sows. Journal of Inner Mongolia Minzu University (Natural Science), 21, 53–56. (in Chinese)

Fasina Y O, Olowo Y L. 2013. Effect of a commercial yeast-based product (Maxigen®) on intestinal villi morphology and growth performance of broiler chickens. International Journal of Poultry Science12, 9–14.

Gentry L R, Fernandez J M, Ward T L, White T W, Southern L L, Bidner T D, Thompson D L, Horohov D W, Chapa A M, Sahlu T. 1999. Dietary protein and chromium tripicolinate in Suffolk wether lambs: Effects on production characteristics, metabolic and hormonal responses, and immune status. Journal of Animal Science77, 1284–1294.

Hayat K, Bodinga B M, Han D, Yang X, Sun Q Z, Aleya L, Abdel-Daim M M, Yang X J. 2020. Effects of dietary inclusion of chromium propionate on growth performance, intestinal health, immune response and nutrient transporter gene expression in broilers. Science of the Total Environment705, 135869.

He Z X, Sun Z H, Yang W Z, Beauchemin K A, Tang S X, Zhou C S, Han X F, Wang M, Kang J H, Tan Z L. 2014. Effects of maternal protein or energy restriction during late gestation on immune status and responses to lipopolysaccharide challenge in postnatal young goats. Journal of Animal Science92, 4856–4864.

Hernández-Castellano L E, Morales-delaNuez A, Sanchez-Macias D, Moreno-Indias I, Torres A, Capote J, Arguello A, Castro N. 2015a. The effect of colostrum source (goat vs. sheep) and timing of the first colostrum feeding (2h vs. 14h after birth) on body weight and immune status of artificially reared newborn lambs. Journal of Dairy Science98, 204–210.

Hernández-Castellano L E, Suarez-Trujillo A, Martell-Jaizme D, Cugno G, Arguello A, Castro N. 2015b. The effect of colostrum period management on BW and immune system in lambs: From birth to weaning. Animal9, 1672–1679.

Huang Y L, Luo Q H, Xiao F, Lin X, Spears J W. 2020. Research note: Responses of growth performance, immune traits, and small intestinal morphology to dietary supplementation of chromium propionate in heat-stressed broilers. Poultry Science99, 5070–5073.

Jia R L, Bao H Y. 2012. Effect of chromium methionine on the reproductive performance of sows. Feed Industry33, 57–58. (in Chinese)

Kegley E B, Spears J W. 1995. Immune response, glucose metabolism, and performance of stressed feeder calves fed inorganic or organic chromium. Journal of Animal Science73, 2721–2726.

Kerr N R, Mossman C W, Chou C H, Bunten J M, Kelty T J, Childs T E, Rector R S, Arnold W D, Grisanti L A, Du X W, Booth F W. 2024. Hindlimb immobilization induces insulin resistance and elevates mitochondrial ROS production in the hippocampus of female rats. Journal of Applied Physiology137, 512–526.

Khan R U, Naz S, Dhama K. 2014. Chromium: Pharmacological applications in heat stressed poultry. International Journal of Pharmacology10, 213–217.

Khanal P, Nielsen M O. 2017. Impacts of prenatal nutrition on animal production and performance: A focus on growth and metabolic and endocrine function in sheep. Journal of Animal Science and Biotechnology8, 1–14.

Kheiri F, Toghyani M. 2009. Effect of different levels of inorganic chromium on performance and immunity of broiler chicks. Journal of Animal and Veterinary Advances8, 1819–1823.

Lashkari S, Habibian M, Jensen S K. 2018. A review on the role of chromium supplementation in ruminant nutrition - effects on productive performance, blood metabolites, antioxidant status, and immunocompetence. Biological Trace Element Research186, 305–321.

Lei K W, Wu H, Spears J W, Lin X, Wang X, Bai X, Huang Y L. 2024. Responses of growth performance, antioxidant function, small intestinal morphology and mRNA expression of jejunal tight junction protein to dietary iron in yellow-feathered broilers. Journal of Integrative Agriculture23, 1329–1337.

Lei X G, Zhu J H, Cheng W H, Bao Y, Ho Y S, Reddi A R, Holmgren A, Arnér E S. 2016. Paradoxical roles of antioxidant enzymes: Basic mechanisms and health implications. Physiological Reviews96, 307–364.

Li X C, Zhao W J, Zhang F F, Chen H C, Feng Q K, Huang S Wang G. 2012. Effect of chromium on the reproductive performance of SPF-rated New Zealand rabbits. Laboratory Animal Science29, 26–28. (in Chinese)

Lien T F, Horng Y M, Yang K H. 1999. Performance, serum characteristics, carcase traits and lipid metabolism of broilers as affected by supplement of chromium picolinate. British Poultry Science40, 357–363.

Lindemann M D, Carter S D, Chiba L I, Dove C R, LeMieux F M, Southern L L. 2004. A regional evaluation of chromium tripicolinate supplementation of diets fed to reproducing sows. Journal of Animal Science82, 2972–2977.

Lloyd K E, Fellner V, McLeod S J, Fry R S, Krafka K, Lamptey A, Spears J W. 2010. Effects of supplementing dairy cows with chromium propionate on milk and tissue chromium concentrations. Journal of Dairy Science93, 4774–4780.

Lu L, Zhao L L, Dong S Y, Liao X D, Dong X Y, Zhang L Y, Luo X G. 2019. Dietary supplementation of organic or inorganic chromium modulates the immune responses of broilers vaccinated with Avian influenza virus vaccine. Animal13, 983–991.

Ma J, Mahfuz S, Wang J, Piao X. 2021. Effect of dietary supplementation with mixed organic acids on immune function, antioxidative characteristics, digestive enzymes activity, and intestinal health in broiler chickens. Frontiers in Nutrition8, 673316.

Mekuriaw Y. 2023. Negative energy balance and its implication on productive and reproductive performance of early lactating dairy cows. Journal of Applied Animal Research51, 220–229.

Moonsie-Shageer S, Mowat D N. 1993. Effect of level of supplemental chromium on performance, serum constituents, and immune status of stressed feeder calves. Journal of Animal Science71, 232–238.

Mousaie A, Valizadeh R, Chamsaz M. 2017. Selenium-methionine and chromium-methionine supplementation of sheep around parturition: Impacts on dam and offspring performance. Archives of Animal Nutrition, 71, 134–149.

Nouri M, Zarrin M, Ahmadpour A, Castro N, González-Cabrera M, Hernández-Castellano L E. 2023. Feed restriction around parturition does not affect colostrum immunoglobulin G concentration in dairy fat-tailed sheep but does affect performance and blood metabolites in newborn lambs. Journal of Dairy Science106, 2980–2988.

NRC (National Research Council). 2007. Nutrient Requirements of Goats. 7th ed. National Academies Press, Washington, D.C.

Pechova A, Pavlata L. 2007. Chromium as an essential nutrient: A review. Veterinarni Medicina52, 1–18.

Ranneh Y, Akim A M, Hamid H A, Khazaai H, Fadel A, Mahmoud A M. 2019. Stingless bee honey protects against lipopolysaccharide induced-chronic subclinical systemic inflammation and oxidative stress by modulating Nrf2, NF-κB and p38 MAPK. Nutrition and Metabolism16, 1–17.

Real D E, Nelssen J L, Tokach M D, Goodband R D, Dritz S S, Woodworth J C, Owen K Q. 2008. Additive effects of L-carnitine and chromium picolinate on sow reproductive performance. Livestock Science116, 63–69.

Rodríguez C, Castro N, Capote J, Morales-DelaNuez A, Moreno-Indias I, Sánchez-Macías D, Argüello A. 2009. Effect of colostrum immunoglobulin concentration on immunity in Majorera goat kids. Journal of Dairy Science92, 1696–1701.

Sahin K, Ozbey O, Onderci M, Cikim G, Aysondu M H. 2002. Chromium supplementation can alleviate negative effects of heat stress on egg production, egg quality and some serum metabolites of laying Japanese quail. The Journal of nutrition132, 1265–1268.

Sahin N, Akdemir F, Tuzcu M, Hayirli A, Smith M O, Sahin K. 2010. Effects of supplemental chromium sources and levels on performance, lipid peroxidation and proinflammatory markers in heat-stressed quails. Animal Feed Science and Technology159, 143–149.

Sahin N, Sahin K, Onderci M, Gursu M F, Cikim G, Vijaya J, Kucuk O. 2005. Chromium picolinate, rather than biotin, alleviates performance and metabolic parameters in heat-stressed quail. British Poultry Science46, 457–463.

Sands J S, Smith M O. 1999. Broilers in heat stress conditions: Effects of dietary manganese proteinate or chromium picolinate supplementation. Journal of Applied Poultry Research8, 280–287

SAS (Statistical Analysis System). 2008. Institute SAS/STAT version 9.2 User's Guide. SAS Institute, Cary, NC, USA.

Seifalinasab A, Mousaie A, Doomary H. 2022. Dietary high chromium-methionine supplementation in summer-exposed finishing lambs: Impacts on feed intake, growth performance, and blood cells, antioxidants, and minerals. Biological Trace Element Research200, 156–163.

Sordillo L M, Aitken S L. 2009. Impact of oxidative stress on the health and immune function of dairy cattle. Veterinary Immunology and Immunopathology128, 104–109.

Spears J W. 2019. Boron, chromium, manganese, and nickel in agricultural animal production. Biological Trace Element Research188, 35–44.

Spears J W, Lloyd K E, Krafka K, Hyda J, Grime J L. 2024. Research note: Chromium propionate for turkeys: Effect on tissue chromium concentrations and human food safety. Poultry Science103, 103196.

Spears J W, Lloyd K E, Pickworth C A, Huang Y L, Krafka K, Hyda J, Grime J L. 2019. Chromium propionate in broilers: Human food and broiler safety. Poultry Science98, 6579–6585.

Spears J W, Lloyd K E, Siciliano P, Pratt-Phillips S, Goertzen E W, McLeod S J, Moore J, Krafka K, Hyda J, Rounds W. 2020. Chromium propionate increases insulin sensitivity in horses following oral and intravenous carbohydrate administration. Journal of Animal Science98, skaa095.

Staniek H, Krejpcio Z. 2009. The effects of tricentric chromium (III) propionate complex supplementation on pregnancy outcome and maternal and foetal mineral status in rat. Food and Chemical Toxicology47, 2673–2678.

Takeuchi Y, Kikusui T, Mori Y. 1995. Changes in the behavioral parameters following the lipopolysaccharide administration in goats. Journal of Veterinary Medical Science57, 1041–1044.

Vincent J B. 2001. The bioinorganic chemistry of chromium (III). Polyhedron20,1–26.

Wang M Q, Wang C, Li H, Du Y J, Tao W J, Ye S S, He Y D. 2012. Effects of chromium-loaded chitosan nanoparticles on growth, blood metabolites, immune traits and tissue chromium in finishing pigs. Biological Trace Element Research149, 197–203.

Zha L Y, Zeng J W, Chu X W, Mao L M, Luo H J. 2009. Efficacy of trivalent chromium on growth performance, carcass characteristics and tissue chromium in heat-stressed broiler chicks. Journal of the Science of Food and Agriculture, 89, 1782–1786.

Zhang L L, Gu X L, Wang J, Liao S, Duan Y H, Li H, Song Z H, He X, Fan Z Y. 2021. Effects of dietary isomaltooligosaccharide levels on the gut microbiota, immune function of sows, and the diarrhea rate of their offspring. Frontiers in Microbiology11, 588986.

Zhang Q Q, Zhang H T, Jiang Y K, Wang J P, Wu D, Wu C M, Che L Q, Lin Y, Zhuo Y, Luo Z, Nie K K, Li J. 2024. Chromium propionate supplementation to energy-and protein-reduced diets reduces feed consumption but improves feed conversion ratio of yellow feathered male broilers in the early period and improves meat quality. Poultry Science103, 103260.

Zhang Y M, Ao D, Lei K W, Lin X, Spears J W, Shi H T, Huang Y L, Yang F L. 2023. Dietary copper supplementation modulates performance and lipid metabolism in meat goat kids. Journal of Integrative Agriculture22, 214–221.

No related articles found!
No Suggested Reading articles found!