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Biological Trace Element Research

, Volume 189, Issue 2, pp 529–537 | Cite as

Organic Chromium Form Alleviates the Detrimental Effects of Heat Stress on Nutrient Digestibility and Nutrient Transporters in Laying Hens

  • Cemal Orhan
  • Mehmet Tuzcu
  • Patrick Brice Defo Deeh
  • Nurhan Sahin
  • James R. Komorowski
  • Kazim SahinEmail author
Article
  • 122 Downloads

Abstract

In the present study, we investigated the effects of chromium-picolinate (CrPic) and chromium-histidinate (CrHis) on nutrient digestibility and nutrient transporters in laying hens exposed to heat stress (HS). Hens (n = 1800; 16 weeks old) were kept in cages in temperature-controlled rooms at either 22 ± 2 °C for 24 h/day (thermoneutral (TN)) or 34 ± 2 °C for 8 h/day, from 08:00 to 17:00, followed by 22 °C for 16 h (HS) for 12 weeks. Hens reared under both environmental conditions were fed one of three diets: a basal diet and the basal diet supplemented with either 1.600 mg of CrPic (12.43% Cr) or 0.788 mg of CrHis (25.22% Cr) per kg of diet, delivering 200 μg elemental Cr per kg of diet. HS impaired the nutrient digestibility and nutrient transports in laying hens (P < 0.001). However, both Cr sources increased digestibility of dry matter (DM; P < 0.001), organic matter (OM; P < 0.05), crude protein (CP; P < 0.001), and crude fat (CF; P < 0.001). Both Cr sources partially alleviated detrimental effects of HS on fatty acid-binding and transport protein1 (FABP1, FATP1), glucose (SGLT1, GLUT1, GLUT10), protein (PepT1, PepT2), and amino acid transporters (ASCT1, bo,+AT1, CAT1, EAAT1, LAT1) of the ileum (P < 0.0001). The efficacy of Cr as CrHis was more notable than Cr as CrPic, which could be attributed to higher bioavailability. Finally, the detrimental effects of HS on nutrient digestibility and nutrient transporters were alleviated by CrPic and CrHis. These findings may justify the use of CrPic and CrHis in poultry.

Keywords

Chromium-histidinate Chromium-picolinate Digestibility Nutrient transporters Heat stress 

Notes

Acknowledgments

Thanks are extended to Farmavet International (İstanbul, Turkey) for donating vitamin-mineral premixes and reconstituting premixes with Cr chelates.

Authors’ Contributions

KS and JRK participated in the study design and drafting the manuscript. VK, CO, MT, HT, MI, HT, and NS participated in the data collection and assays, data analysis, and drafting the manuscript. VK and DDPB participated in the data analysis and statistical analysis for the variables and drafting the manuscript. KS and JRK participated in drafting the manuscript. All authors read and approved the final manuscript.

Funding

The study was funded by Small and Medium Business Development and Support Administration of Turkey (KOSGEB) and also in part by Turkish Academy of Sciences (Ankara, Turkey). The authors thank Nutrition 21 (NY, USA) for providing chromium picolinate and chromium histidinate.

Compliance with Ethical Standards

All animal experimental procedures followed protocols approved by the Institutional Animal Ethics Committee of Veterinary Control Institute (Elazig, Turkey).

Conflict of Interest

The authors declare that there are no conflicts of interest. James R. Komorowski is an employee of Nutrition 21, Inc., NY, USA.

References

  1. 1.
    Windhorst HW (2006) Changes in poultry production and trade worldwide. World’s Poult Sci J 62:585–602Google Scholar
  2. 2.
    Lara LJ (2013) Rostagno MH impact of heat stress on poultry production. Animals 3:356–369Google Scholar
  3. 3.
    Sahin K, Onderci M, Sahin N, Gursu MF, Khachik F, Kucuk O (2006) Effects of lycopene supplementation on antioxidant status, oxidative stress, performance and carcass characteristics in heat-stressed Japanese quail. J Therm Biol 31(4):307–312Google Scholar
  4. 4.
    Tumová E, Gous RM (2012) Interaction of hen production type, age, and temperature on laying pattern and egg quality. Poult Sci 91:1269–1275Google Scholar
  5. 5.
    Payne CG (1966) Practical aspects of environmental temperature for laying hens. Worlds Poult Sci J 22(2):126–139Google Scholar
  6. 6.
    Bahadoran S, Dehghani Samani A, Hassanpour H (2018) Effect of heat stress on the gene expression of ion transporters/channels in the uterus of laying hens during eggshell formation. Stress 21(1):51–58Google Scholar
  7. 7.
    Ozdemir O, Tuzcu M, Sahin N, Orhan C, Tuzcu Z, Sahin K (2017) Organic chromium modifies the expression of orexin and glucose transporters of ovarian in heat-stressed laying hens. Cell Mol Biol (Noisy-le-grand) 63(10):93–98Google Scholar
  8. 8.
    Zerjal T, Gourichon D, Rivet B, Bordas A (2013) Performance comparison of laying hens segregating for the frizzle gene under thermoneutral and high ambient temperatures. Poult Sci 92(6):1474–1485Google Scholar
  9. 9.
    Sahin N, Hayirli A, Orhan C, Tuzcu M, Komorowski JR, Sahin K (2018) Effects of the supplemental chromium form on performance and metabolic profile in laying hens exposed to heat stress. Poult Sci 97(4):1298–1305Google Scholar
  10. 10.
    Ebeid TA, Suzuki T, Sugiyama T (2012) High ambient temperature influences eggshell quality and calbindin-D28k localization of eggshell gland and all intestinal segments of laying hens. Poult Sci 91(9):2282–2287Google Scholar
  11. 11.
    Torki M, Zangeneh S, Habibian M (2014) Performance, egg quality traits, and serum metabolite concentrations of laying hens affected by dietary supplemental chromium picolinate and vitamin C under a heat-stress condition. Biol Trace Elem Res 157(2):120–129Google Scholar
  12. 12.
    Abd El-Hack ME, Mahrose K, Askar AA, Alagawany M, Arif M, Saeed M, Abbasi F, Soomro RN, Siyal FA, Chaudhry MT (2017) Single and combined impacts of vitamin A and selenium in diet on productive performance, egg quality, and some blood parameters of laying hens during hot season. Biol Trace Elem Res 177(1):169–179Google Scholar
  13. 13.
    Mashaly MM, Hendricks GL 3rd, Kalama MA, Gehad AE, Abbas AO, Patterson PH (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci 83(6):889–894Google Scholar
  14. 14.
    Deng W, Dong XF, Tong JM, Zhang Q (2012) The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult Sci 91(3):575–582Google Scholar
  15. 15.
    Koelkebeck KW, Parsons CM, Wang X (1998) Effect of acute heat stress on amino acid digestibility in laying hens. Poult Sci 77(9):1393–1396Google Scholar
  16. 16.
    Geraert PA, Padilha JCF, Guillaumin S (1996) Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. Br J Nutr 75:195–204Google Scholar
  17. 17.
    Ferrer C, Pedragosa E, Torras-Llort M, Parcerisa X, Rafecas M, Ferrer R, Amat C, Moretó M (2003) Dietary lipidsmodify brush border membrane composition and nutrient transport in chicken small intestine. J Nutr 133:1147–1153Google Scholar
  18. 18.
    Shepherd EJ, Helliwell PA, Mace OJ, Morgan EL, Patel N, Kellett GL (2004) Stress and glucocorticoid inhibit apical Glut2-trafficking and intestinal glucose absorption in rat small intestine. J Physiol 560:281–290Google Scholar
  19. 19.
    McArthur MJ, Atshaves BP, Frolov A, Foxworth WD, Kier AB, Schroeder F (1999) Cellular uptake and intracellular trafficking of long chain fatty acids. J Lipid Res 40:1371–1383Google Scholar
  20. 20.
    Furuhashi M, Hotamisligil GS (2008) Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 7:489–503Google Scholar
  21. 21.
    Habashy WS, Milfort MC, Fuller AL, Attia YA, Rekaya R, Aggrey SE (2017) Effect of heat stress on protein utilization and nutrient transporters in meat-type chickens. Int J Biometeorol 61:2111–2118.  https://doi.org/10.1007/s00484-017-1414-1 Google Scholar
  22. 22.
    Braun E, Sweazea KL (2008) Glucose regulation in birds. Comp Biochem Physiol B Biochem Mol Biol 151:1–9Google Scholar
  23. 23.
    Steel A, Hediger MA (1998) The molecular physiology of sodium and proton-coupled solute transporters. News Physiol Sci 13:123–131Google Scholar
  24. 24.
    Daniel H, Kottra G (2004) The proton oligopeptide cotransporter family SLC15 in physiology and pharmacology. Pflügers Arch-Eur J Physiol 447:610–618Google Scholar
  25. 25.
    Lien TF, Chen KL, Wu CP, Lu JJ (2004) Effects of supplemental copper and chromium on the serum and egg traits of laying hens. Br Poult Sci 45:535–539Google Scholar
  26. 26.
    Ziegenfuss TN, Lopez HL, Kedia A, Habowski SM, Sandrock JE, Raub B, Kerksick CM, Ferrando AA (2017) Effects of an amylopectin and chromium complex on the anabolic response to a suboptimal dose of whey protein. J Int Soc Sports Nutr 8(14):6Google Scholar
  27. 27.
    Sahin K, Tuzcu M, Smith MO, Sahin N (2009) Chromium supplementation: a tool for alleviation of thermal stress in poultry. CAB Rev: Perspect Agric, Vet Sci, Nutr Nat Resour 4:1–11Google Scholar
  28. 28.
    Sahin N, Akdemir F, Tuzcu M, Hayirli A, Smith MO, Sahin K (2010) Effects of supplemental chromium sources and levels on performance, lipid peroxidation and proinflammatory markers in heat-stressed quails. Anim Feed Sci Technol 159:143–149Google Scholar
  29. 29.
    Cupo MA, Donaldson WE (1987) Chromium and vanadium effects on glucose metabolism and lipid synthesis in the chick. Poult Sci 66:120–126Google Scholar
  30. 30.
    Hayirli A (2005) Chromium nutrition of livestock species. Nutr. Abs. Rev. Ser B: Livest Feeds Feed 75:1–14Google Scholar
  31. 31.
    EEC (1986) Council Directive 86/609/EEC of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes. OJEC 358:1–29Google Scholar
  32. 32.
    AOAC (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists. Washington, DC.USAGoogle Scholar
  33. 33.
    Onderci M, Sahin N, Sahin K, Kilic N (2003) Antioxidant properties of chromium and zinc: in vivo effects on digestibility, lipid peroxidation, antioxidant vitamins, and some minerals under a low ambient temperature. Biol Trace Elem Res 92:139–150Google Scholar
  34. 34.
    Sahin K, Tuzcu M, Orhan C, Sahin N, Kucuk O, Ozercan IH, Juturu V, Komorowski JR (2013) Anti-diabetic activity of chromium picolinate and biotin in rats with type 2 diabetes induced by high-fat diet and streptozotocin. Br J Nutr 110:197–205Google Scholar
  35. 35.
    Xiaozhen S, Junrong L, Daibo F, Xianghui Z, Kornmatitsuk B, Zhensong X, Mingren Q (2014) Traditional Chinese medicine prescriptions enhance growth performance of heat stressed beef cattle by relieving heat stress responses and increasing apparent nutrient digestibility. Asian-Australas J Anim Sci 27(10):1513–1520Google Scholar
  36. 36.
    Brijesh Y, Gyanendra S, Alok W, Dutta N, Chaturvedi VB, Verma MR (2016) Effect of simulated heat stress on digestibility, methane emission and metabolic adaptability in crossbred cattle. Asian-Australas J Anim Sci 29(11):1585–1592Google Scholar
  37. 37.
    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 91:2235–2240Google Scholar
  38. 38.
    Diarra SS, Tabuaciri P (2014) Feeding management of poultry in high environmental temperatures. Int J Poult Sci 13:657–661Google Scholar
  39. 39.
    Lamson DW, Plaza SM (2002) The safety and efficacy of high-dose chromium. Altern Med Rev 7(3):218–235Google Scholar
  40. 40.
    Anderson RA, Polansky MM, Bryden NA (2004) Stability and absorption of chromium and absorption of chromium histidinate complexes by humans. Biol Trace Elem Res 101:211–218Google Scholar
  41. 41.
    Bonnet S, Geraert PA, Lessire M, Carre B, Guillaumin S (1997) Effect of high ambient temperature on feed digestibility in broilers. Poult Sci 76:857–863Google Scholar
  42. 42.
    Turcotte LP, Srivastava AK, Chiasson JL (1997) Fasting increases plasma membrane fatty acid-binding protein (FABP (PM)) in red skeletal muscle. Mol Cell Biochem 166:153–158Google Scholar
  43. 43.
    Sun X, Zhang H, Sheikhahmadi A, Wang Y, Jiao H, Lin H, Song Z (2015) Effects of heat stress on the gene expression of nutrient transporters in the jejunum of broiler chickens (Gallus gallus domesticus). Int J Biometeorol 59:127–135Google Scholar
  44. 44.
    Stahl A (2004) A current review of fatty acid transport proteins (SLC27). Pflügers Arch-Eur J Physiol 447:722–727Google Scholar
  45. 45.
    Harada N, Inagaki N (2012) Role of sodium-glucose transporters in glucose uptake of the intestine and kidney. J Diabetes Investig 3:352–353Google Scholar
  46. 46.
    Gorboulev V, Schürmann A, Vallon V, Kipp H, Jaschke A, Klessen D, Friedrich A, Scherneck S, Rieg T, Cunard R, Veyhl-Wichmann M, Srinivasan A, Balen D, Breljak D, Rexhepaj R, Parker HE, Gribble FM, Reimann F, Lang F, Wiese S, Sabolic I, Sendtner M, Koepsell H (2012) Na+−D-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes 61:187–196Google Scholar
  47. 47.
    Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, Rhoads RP, Baumgard LH, Gabler NK (2013) Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8(8):e70215.  https://doi.org/10.1371/journal.pone.0070215 Google Scholar
  48. 48.
    Mahmoud KZ, Edens FW (2003) Influence of selenium source on age related and mild heat stress related changes of blood and liver glutathione redox cycle in broiler chickens (Gallus domesticus). Comp Biochem Physiol B Biochem Mol Biol 136:921–934Google Scholar
  49. 49.
    Bánhegyi G, Benedetti A, Margittai É, Marcolongo P, Fulceri R, Németh CE, Szarka A (2014) Subcellular compartmentation of ascorbate and its variation in disease states. Biochim Biophys Acta 1843:1909–1916Google Scholar
  50. 50.
    Yi-Ching L, Hsun-Yi H, Chia-Jung C, Chao-Hung C, Yuan-Tsong C (2010) Mitochondrial GLUT10 facilitates dehydroascorbic acid import and protects cells against oxidative stress: mechanistic insight into arterial tortuosity syndrome. Hum Mol Genet 19(19):3721–3733Google Scholar
  51. 51.
    Muñoz-Montesino C, Roa FJ, Peña E, González M, Sotomayor K, Inostroza E, Muñoz CA, González I, Maldonado M, Soliz C, Reyes AM, Vera JC, Rivas CI (2014) Mitochondrial ascorbic acid transport is mediated by a low-affinity form of the sodium-coupled ascorbic acid transporter-2. Free Radic Biol Med 70:241–254Google Scholar
  52. 52.
    Syu YW, Lai HW, Jiang CL, Tsai HY, Lin CC, Lee YC (2018) GLUT10 maintains the integrity of major arteries through regulation of redox homeostasis and mitochondrial function. Hum Mol Genet 27(2):307–321Google Scholar
  53. 53.
    Chen G, Liu P, Pattar GR, Tackett L, Bhonagiri P, Strawbridge AB, Elmendorf JS (2006) Chromium activates glucose transporter 4 trafficking and enhances insulin-stimulated glucose transport in 3t3-l1 adipocytes via a cholesterol-dependent mechanism. Mol Endocrinol 20(4):857–870Google Scholar
  54. 54.
    Zwarycz B, Wong EA (2013) Expression of the peptide transporters PepT1, PepT2, and PHT1 in the embryonic and post hatch chick. Poult Sci 92:1314–1321Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Animal Nutrition, Faculty of Veterinary ScienceFirat UniversityElazigTurkey
  2. 2.Division of Biology, Faculty of ScienceFirat UniversityElazigTurkey
  3. 3.Department of Animal Biology, Faculty of Science, Animal Physiology and Phytopharmacology LaboratoryUniversity of DschangDschangCameroon
  4. 4.Research & Development, Nutrition 21 Inc., PurchaseNew YorkUSA

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