Skip to main content
SpringerLink
Log in

Protective effects of dietary mannan oligosaccharide on heat stress–induced hepatic damage in broilers

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Heat stress is a major concern in broiler’s production, which can damage liver of broilers. This study investigated the protective effects of mannan oligosaccharide (MOS) on heat stress–induced hepatic injury in broilers. A total of 144 day-old male chicks were allocated into three treatment groups. Broilers raised under normal ambient temperature were fed a basal diet (control group), and broilers under heat stress (32–33 °C for 8 h daily) were given the basal diet supplemented without MOS (heat stress group) or with 1 g/kg MOS (MOS group) for 42 days. Compared with the control group, heat stress reduced liver weight, whereas increased aspartate aminotransferase (AST) and alanine aminotransferase (ALT) activities in the serum. It also reduced glutathione peroxidase (GSH-Px) activity in the serum and liver, GSH content, and superoxide dismutase (SOD) activity in the liver, but increased malondialdehyde (MDA) concentration in the serum and liver. Dietary MOS decreased serum ALT activity in heat-stressed broilers. MOS inclusion also decreased serum MDA content, but elevated hepatic GSH-Px and SOD activities, with MDA content and GSH-Px activity still being different from the control group, and SOD activity being similar to the control group. Heat stress increased concentrations of tumor necrosis factor α (TNF-α) in the serum and liver, interleukin-1β (IL-1β) in the liver, and mRNA abundances of HSP70, TLR4, MyD88, TNF-α, and IL-1β in the liver of broilers. Serum TNF-α content and mRNA abundances of hepatic TLR4 and TNF-α in MOS group were lower than the heat stress group, whereas these indexes were still higher than the control group. Our results indicated that dietary MOS ameliorated hepatic damage in heat-stressed broilers through alleviation of oxidative stress and inflammation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • AL-Sagan AA, Khalil S, Hussein EOS, Attia YA (2020) Effects of fennel seed powder supplementation on growth performance, carcass characteristics, meat quality, and economic efficiency of broilers under thermoneutral and chronic heat stress conditions. Animals 10:206

    Google Scholar 

  • Ari ZB, Avlas O, Pappo O, Zilbermints V, Cheporko Y, Bachmetov L, Zemel R, Shainberg A, Sharon E, Grief F (2012) Reduced hepatic injury in toll-like receptor 4-deficient mice following d-galactosamine/lipopolysaccharide-induced fulminant hepatic failure. Cell Physiol Biochem 29:41–50

    Google Scholar 

  • Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, Usman MM, Ijaz S, Rehman H (2013) Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. J Anim Physiol Anim Nutr 97:68–73

    Google Scholar 

  • Attia YA, Al-Hamid AA, Ibrahim MS, Al-Harthi MA, Bovera F, Elnaggar AS (2014) Productive performance, biochemical and hematological traits of broiler chickens supplemented with propolis, bee pollen, and mannan oligosaccharides continuously or intermittently. Livest Sci 164:87–95

    Google Scholar 

  • Attia YA, Al-Khalaifah H, Ibrahim MS, Al-Hamid AEA, Al-Harthi MA, El-Naggar A (2017) Blood hematological and biochemical constituents, antioxidant enzymes, immunity and lymphoid organs of broiler chicks supplemented with propolis, bee pollen and mannan oligosaccharides continuously or intermittently. Poult Sci 96:4182–4192

    CAS  Google Scholar 

  • Attia YA, Abd El-Hamid AE, Abdallah AA, Berikaa MA, El-Gandy MF, Sahin K, Abou-Shehema BM (2018a) Effect of betaine, vitamin C and vitamin E on egg quality, hatchability, and markers of liver and renal functions in dualpurpose breeding hens exposed to chronic heat stress. Eur Poult Sci 82:1–15

  • Attia YA, Al-Harthi MA, Sh Elnaggar A (2018b) Productive, physiological and immunological responses of two broiler strains fed different dietary regimens and exposed to heat stress. Ital J Anim Sci 17:686–697

    CAS  Google Scholar 

  • Attia YA, El-Naggar AS, Abou-Shehema BM, Abdella AA (2019) Effect of supplementation with trimethylglycine (betaine) and/or vitamins on semen quality, fertility, antioxidant status, DNA repair and welfare of roosters exposed to chronic heat stress. Animals 9:547

    Google Scholar 

  • Baurhoo B, Ferket PR, Zhao X (2009) Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, cecal and litter microbial populations, and carcass parameters of broilers. Poult Sci 88:2262–2272

    CAS  Google Scholar 

  • Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5(1):9–19

    CAS  Google Scholar 

  • Bozkurt M, Tokuşoğlu Ö, Küçükyilmaz K, Akşit H, Çabuk M, Uğur Çatli A, Seyrek K, Çinar M (2012) Effects of dietary mannan oligosaccharide and herbal essential oil blend supplementation on performance and oxidative stability of eggs and liver in laying hens. Ital J Anim Sci 11:223–229

    CAS  Google Scholar 

  • Che TM, Johnson RW, Kelley KW, Dawson KA, Moran CA, Pettigrew JE (2012a) Effects of mannan oligosaccharide on cytokine secretions by porcine alveolar macrophages and serum cytokine concentrations in nursery pigs. J Anim Sci 90:657–668

    CAS  Google Scholar 

  • Che TM, Song M, Liu Y, Johnson RW, Kelley KW, Van Alstine WG, Dawson KA, Pettigrew JE (2012b) Mannan oligosaccharide increases serum concentrations of antibodies and inflammatory mediators in weanling pigs experimentally infected with porcine reproductive and respiratory syndrome virus. J Anim Sci 90:2784–2793

    CAS  Google Scholar 

  • Chen H, Yan X, Zhu P, Lin J (2006) Antioxidant activity and hepatoprotective potential of agaro-oligosaccharides in vitro and in vivo. Nutr J 5:31

    Google Scholar 

  • Chen HL, Wang CH, Kuo YW, Tsai CH (2010) Antioxidative and hepatoprotective effects of fructo-oligosaccharide in d-galactose-treated Balb/cJ mice. Br J Nutr 105:805–809

    Google Scholar 

  • Chen YP, Zhang H, Cheng YF, Li YH, Wen C, Zhou YM (2018) Dietary L-threonine supplementation attenuates lipopolysaccharide-induced inflammatory responses and intestinal barrier damage of broiler chickens at an early age. Br J Nutr 119:1254–1262

    CAS  Google Scholar 

  • Cheng YF, Du MF, Xu Q, Chen YP, Wen C, Zhou YM (2018) Dietary mannan oligosaccharide improves growth performance, muscle oxidative status, and meat quality in broilers under cyclic heat stress. J Therm Biol 75:106–111

    CAS  Google Scholar 

  • Cheng YF, Chen YP, Chen R, Su Y, Zhang RQ, He QF, Wang K, Wen C, Zhou YM (2019) Dietary mannan oligosaccharide ameliorates cyclic heat stress-induced damages on intestinal oxidative status and barrier integrity of broilers. Poult Sci 98:4767–4776

    CAS  Google Scholar 

  • Cheng YF, Chen YP, Li J, Qu HM, Zhao YR, Wen C, Zhou YM (2020) Dietary β-sitosterol regulates serum lipid level and improves immune function, antioxidant status, and intestinal morphology in broilers. Poult Sci 99:1400–1408

    Google Scholar 

  • De los Santos FS, Donoghue AM, Farnell MB, Huff GR, Huff WE, Donoghue DJ (2007) Gastrointestinal maturation is accelerated in turkey poults supplemented with a mannan-oligosaccharide yeast extract (Alphamune). Poult Sci 86:921–930

    Google Scholar 

  • Feng J, Zhang M, Zheng S, Xie P, Ma A (2008) Effects of high temperature on multiple parameters of broilers in vitro and in vivo. Poult Sci 87:2133–2139

    CAS  Google Scholar 

  • Halas V, Nochta I (2012) Mannan oligosaccharides in nursery pig nutrition and their potential mode of action. Animals 2:261–274

    Google Scholar 

  • Heinrichs AJ, Jones CM, Heinrichs BS (2003) Effects of mannan oligosaccharide or antibiotics in neonatal diets on health and growth of dairy calves. J Dairy Sci 86:4064–4069

    CAS  Google Scholar 

  • Hoek JB, Pastorino JG (2002) Ethanol, oxidative stress, and cytokine-induced liver cell injury. Alcohol 27:63–68

    CAS  Google Scholar 

  • Huang SC, Fu YF, Rehman MU, Li K, Lan YF, Liu W, Luo HQ, Zhang H, Zhang LH, Hao YN, Tong ZX (2018) Effect of the acute heat stress on serum endotoxin concentration and the expression of TLR4 mRNA in liver of Arbor Acres broiler chickens. Anim Prod Sci 58:2200–2206

    Google Scholar 

  • Jastrebski SF, Lamont SJ, Schmidt CJ (2017) Chicken hepatic response to chronic heat stress using integrated transcriptome and metabolome analysis. PLoS One 12:e0181900

    Google Scholar 

  • Jazi V, Foroozandeh AD, Toghyani M, Dastar B, Rezaie Koochaksaraie R, Toghyani M (2018) Effects of Pediococcus acidilactici, mannan-oligosaccharide, butyric acid and their combination on growth performance and intestinal health in young broiler chickens challenged with Salmonella Typhimurium. Poult Sci 97:2034–2043

    CAS  Google Scholar 

  • Kang MG, Lee HJ, Cho JY, Kim K, Yang SJ, Kim D (2016) Anti-inflammatory effects of sucrose-derived oligosaccharides produced by a constitutive mutant L. mesenteroides B-512FMCM dextransucrase in high fat diet-fed mice. Biochem Biophys Res Commun 477:350–355

    CAS  Google Scholar 

  • Khan RU, Naz S, Nikousefat Z, Tufarelli V, Javdani M, Rana N, Laudadio V (2011) Effect of vitamin E in heat-stressed poultry. Worlds Poult Sci J 67(3):469–478

    Google Scholar 

  • Khan RU, Naz S, Nikousefat Z, Selvaggi M, Laudadio V, Tufarelli V (2012) Effect of ascorbic acid in heat-stressed poultry. Worlds Poult Sci J 68(3):477–490

    Google Scholar 

  • Kim GB, Seo YM, Kim CH, Paik IK (2011) Effect of dietary prebiotic supplementation on the performance, intestinal microflora, and immune response of broilers. Poult Sci 90:75–82

    CAS  Google Scholar 

  • Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci 87:E101–E108

    CAS  Google Scholar 

  • Lara JL, Rostagno HM (2013) Impact of heat stress on poultry production. Animals 3:356–369

    Google Scholar 

  • Lin H, Decuypere E, Buyse J (2006) Acute heat stress induces oxidative stress in broiler chickens. Comp Biochem Physiol A Mol Integr Physiol 144:11–17

    Google Scholar 

  • Liu B, Xu L, Ge X, Xie J, Xu P, Zhou Q, Pan L, Zhang Y (2013) Effects of mannan oligosaccharide on the physiological responses, HSP70 gene expression and disease resistance of Allogynogenetic crucian carp (Carassius auratus gibelio) under Aeromonas hydrophila infection. Fish Shellfish Immunol 34:1395–1403

    CAS  Google Scholar 

  • Liu L, Shen J, Zhao C, Wang X, Yao J, Gong Y, Yang X (2015) Dietary Astragalus polysaccharide alleviated immunological stress in broilers exposed to lipopolysaccharide. Int J Biol Macromol 72:624–632

    CAS  Google Scholar 

  • Liu HW, Li K, Zhao JS, Deng W (2017) Effects of chestnut tannins on intestinal morphology, barrier function, pro-inflammatory cytokine expression, microflora and antioxidant capacity in heat-stressed broilers. J Anim Physiol Anim Nutr 102:717–726

    Google Scholar 

  • NRC (1994) Nutrient requirements of poultry, 9th revion edition. Natl Acad Press, Washington, DC

    Google Scholar 

  • O’Neill LAJ (2006) How Toll-like receptors signal: what we know and what we don’t know. Curr Opin Immunol 18:3–9

    Google Scholar 

  • Pourabedin M, Xu Z, Baurhoo B, Chevaux E, Zhao X (2014) Effects of mannan oligosaccharide and virginiamycin on the cecal microbial community and intestinal morphology of chickens raised under suboptimal conditions. Can J Microbiol 60:255–266

    CAS  Google Scholar 

  • Qiao Y, Bai XF, Du YG (2011) Chitosan oligosaccharides protect mice from LPS challenge by attenuation of inflammation and oxidative stress. Int Immunopharmacol 11:121–127

    CAS  Google Scholar 

  • Sahin K, Orhan C, Tuzcu Z, Tuzcu M, Sahin N (2012) Curcumin ameloriates heat stress via inhibition of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem Toxicol 50:4035–4041

    CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    CAS  Google Scholar 

  • Şenay S, Islim P, Tugay A (2019) Supplementation of natural antioxidants to reduced crude protein diets for Japanese quails exposed to heat stress. Braz J Poult Sci 21(1):001–014

    Google Scholar 

  • Sohail MU, Ijaz A, Yousaf MS, Ashraf K, Zaneb H, Aleem M, Rehman H (2010) Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poult Sci 89:1934–1938

    CAS  Google Scholar 

  • Sohail MU, Hume ME, Byrd JA, Nisbet DJ, Ijaz A, Sohail A, Shabbir MZ, Rehman H (2012) Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult Sci 91:2235–2240

    CAS  Google Scholar 

  • Sohail MU, Ijaz A, Younus M, Shabbir MZ, Kamran Z, Ahmad S, Anwar H, Yousaf MS, Ashraf K, Shahzad AH, Rehman H (2013) Effect of supplementation of mannan oligosaccharide and probiotic on growth performance, relative weights of viscera, and population of selected intestinal bacteria in cyclic heat-stressed broilers. J Appl Poult Res 22:485–491

    CAS  Google Scholar 

  • Song J, Jiao LF, Xiao K, Luan ZS, Hu CH, Shi B, Zhan XA (2013) Cello-oligosaccharide ameliorates heat stress-induced impairment of intestinal microflora, morphology and barrier integrity in broilers. Anim Feed Sci Technol 185:175–181

    CAS  Google Scholar 

  • Song Z, Cheng K, Zhang L, Wang T (2017) Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat-stressed broilers. J Therm Biol 69:184–190

    CAS  Google Scholar 

  • Sun Y, Su J, Yang S, Liu Z, Liu D, Gan F, Chen X, Huang K (2019) Mannan oligosaccharide protects against the aflatoxin-B1-promoted influenza replication and tissue damages in a toll-like-receptor-4-dependent manner. J Agric Food Chem 67:735–745

    CAS  Google Scholar 

  • Tan GY, Yang L, Fu YQ, Feng JH, Zhang MH (2010) Effects of different acute high ambient temperatures on function of hepatic mitochondrial respiration, antioxidative enzymes, and oxidative injury in broiler chickens. Poult Sci 89:115–122

    CAS  Google Scholar 

  • Torrecillas S, Makol A, Betancor MB, Montero D, Caballero MJ, Sweetman J, Izquierdo M (2013) Enhanced intestinal epithelial barrier health status on European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 34:1485–1495

    CAS  Google Scholar 

  • Tufail M, Chand N, Shakoor A, Khan RU, Mobashar M, Naz S (2019) Mannanoligosaccharide (MOS) in broiler diet during the finisher phase: 2. Growth traits and intestinal histomorphology. Pakistan J Zool 51(2):597–602

    Google Scholar 

  • ur Rehman Z, Chand N, Khan RU (2017) The effect of vitamin E, L-carnitine, and ginger on production traits, immune response, and antioxidant status in two broiler strains exposed to chronic heat stress. Environ Sci Pollut Res 24(34):26851–26857

    CAS  Google Scholar 

  • Varasteh S, Braber S, Akbari P, Garssen J, Fink-Gremmels J (2015) Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLoS One 10:e0138975

    Google Scholar 

  • Wan X, Jiang L, Zhong H, Lu Y, Zhang L, Wang T (2017a) Effects of enzymatically treated Artemisia annua L. on growth performance and some blood parameters of broilers exposed to heat stress. Anim Sci J 88:1239–1246

    CAS  Google Scholar 

  • Wan X, Zhang J, He J, Bai K, Zhang L, Wang T (2017b) Dietary enzymatically treated Artemisia annua L. supplementation alleviates liver oxidative injury of broilers reared under high ambient temperature. Int J Biometeorol 61:1629–1636

    Google Scholar 

  • Wang W, Li Z, Han Q, Guo Y, Zhang B, D’inca R (2016) Dietary live yeast and mannan-oligosaccharide supplementation attenuate intestinal inflammation and barrier dysfunction induced by Escherichia coli in broilers. Br J Nutr 116:1878–1888

    CAS  Google Scholar 

  • Wang WC, Yan FF, Hu JY, Amen OA, Cheng HW (2018) Supplementation of Bacillus subtilis-based probiotic reduces heat stress-related behaviors and inflammatory response in broiler chickens. J Anim Sci 96:1654–1666

    CAS  Google Scholar 

  • Wu QJ, Liu N, Wu XH, Wang GY, Lin L (2018) Glutamine alleviates heat stress-induced impairment of intestinal morphology, intestinal inflammatory response, and barrier integrity in broilers. Poult Sci 97:2675–2683

    CAS  Google Scholar 

  • Yang L, Tan GY, Fu YQ, Feng JH, Zhang MH (2010) Effects of acute heat stress and subsequent stress removal on function of hepatic mitochondrial respiration, ROS production and lipid peroxidation in broiler chickens. Comp Biochem Physiol C Toxicol Pharmacol 151:204–208

    Google Scholar 

  • Zdunczyk Z, Juskiewicz J, Jankowski J, Biedrzycka E, Koncicki A (2005) Metabolic response of the gastrointestinal tract of turkeys to diets with different levels of mannan-oligosaccharide. Poult Sci 84:903–909

    CAS  Google Scholar 

  • Zhao PY, Jung JH, Kim IH (2012) Effect of mannan oligosaccharides and fructan on growth performance, nutrient digestibility, blood profile, and diarrhea score in weanling pigs. J Anim Sci 90:833–839

    CAS  Google Scholar 

  • Zheng C, Li F, Hao Z, Liu T (2018) Effects of adding mannan oligosaccharides on digestibility and metabolism of nutrients, ruminal fermentation parameters, immunity, and antioxidant capacity of sheep. J Anim Sci 96:284–292

    Google Scholar 

Download references

Author information

Author notes

  1. Yueping Chen and Yefei Cheng contributed equally to this work.

Authors and Affiliations

  1. College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, People’s Republic of China

    Yueping Chen, Yefei Cheng, Chao Wen & Yanmin Zhou

Authors
  1. Yueping Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yefei Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chao Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanmin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yanmin Zhou.

Ethics declarations

The experimental design and research procedures involving broilers in this study were approved by the Animal Care and Use Committee of Nanjing Agricultural University (Certification No.: SYXK (Su) 2011-0036, 11 August 2015).

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Y., Cheng, Y., Wen, C. et al. Protective effects of dietary mannan oligosaccharide on heat stress–induced hepatic damage in broilers. Environ Sci Pollut Res 27, 29000–29008 (2020). https://doi.org/10.1007/s11356-020-09212-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-09212-2

Keywords

Search

Navigation