Effect of different forms of chromium on feed intake, rumen parameters, and blood metabolites of Afshari ewes during transition period and their lambs under the influence of heat stress

Document Type : Research Paper

Authors

1 Ph.D. Student, Department of Animal and Poultry Nutrition, Faculty of Animal Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

2 Professor, Department of Animal and Poultry Nutrition, Faculty of Animal Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

3 Assistant Professor, Department of Animal and Poultry Nutrition, Faculty of Animal Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

Abstract

Introduction: During the time around parturition, animals make many metabolic adjustments to support the transition from pregnancy to lactation. Before giving birth, animals are subjected to a lot of metabolic effects, to prepare the physiological conditions of the body in the time after giving birth and during lactation. In addition, dairy cattle produce milk more than their ability to consume energy, as a result, they are in a negative energy balance at the beginning of lactation, which may reduce the longevity of the cattle in the herd and increase the rate of elimination of dairy cattle. Heat stress in late pregnancy is aggravated by energy restriction. In such conditions, the use of management and nutritional methods will reduce the problems during the transfer period and heat stress. One of the ways to optimize the productive and reproductive conditions of livestock, through improving the metabolism of nutrients and eliminating or reducing stress conditions, is to use chromium as a metabolic improver. According to scientific sources, the chromium requirement for sheep is three to five mg per day, and for dairy cows is 15 to 50 mg per day. Inorganic chromium has a bioavailability of about 0.5%. Organic chromium has more than 25% intestinal absorption, and therefore, consumption of inorganic chromium is not recommended due to its low bioavailability and toxic effects. Among the sources of organic chromium, chromium-methionine has been recognized by important global food and drug organizations as a compound with high bioavailability, impressive metabolic responses, and no toxicity complications. This experiment was conducted to investigate the effect of using different forms of chromium around calving on feed consumption, nutrient digestibility, nutritional behavior of Afshari ewes, and the performance of their lambs under the influence of heat stress.
Materials and methods: Forty pregnant Afshari ewes were assigned to four experimental treatments with 10 replicates from 42±5 days before the expected birth in a completely randomized design. Experimental treatments include 1) a basic diet without chromium supplementation (control), 2) a basic diet containing three mg of chromium in mineral form per kg of dry matter, 3) a basic diet containing three mg of chromium in the form of chromium-methionine per kg of dry matter, and 4) a basic diet contained three mg of chromium in the form of chromium nanoparticles per kilogram of dry matter. The length of the test period was 84 days. Weighing of ewes was done at the beginning, at the time of calving, and the end of the period. The rest of the feed is weighed every day and the daily feed consumption was calculated by deducting from the provided feed. Sampling of the rumen fluid was done on the 14th day after birth. The rumen fluid was taken before feeding in the morning (zero hour), and at three and six hours after feeding by esophageal tube, then the pH amount of rumen contents was measured and recorded immediately after extraction by a mobile digital pH meter (Metrohm laboratory pH meter-691) which was calibrated at the same place. To measure rumen liquid ammonia nitrogen, samples were used three hours after morning feeding. To measure the concentration of volatile fatty acids, five mL of rumen fluid samples were prepared and 1 mL of metaphosphoric acid 25% was added to them and kept at -20ºC until the experiment. On the 10th day after birth, blood samples were taken from the jugular vein of ewes and lambs three hours after morning feeding. To measure blood metabolites including glucose, insulin, cholesterol, triglyceride, urea, creatinine, total protein, albumin, and globulin, Pars Azmoun chemical kits and auto-analyzer (Spain BT 3500) were used.
Results and discussion: The results showed that, from the third to the sixth weeks after birth, dry matter consumption in ewes receiving chromium-methionine and chromium nanoparticles had an upward trend compared to the other two treatments (P<0.05). The addition of chromium to the diet of ewes had no significant effect on rumen pH, volatile fatty acids, and rumen ammonia nitrogen concentration. The addition of chromium supplement to the diet of ewes caused a significant decrease in the rumen protozoa population compared to the control group (P<0.05). Adding different forms of chromium to the diet of sheep caused a decrease in glucose concentration, and an increase in chromium, insulin, total protein, albumin, and serum globulin compared to the control group (P<0.05). No significant difference was observed between experimental treatments on blood cholesterol, triglyceride, urea, and creatinine concentrations. Also, different forms of chromium did not have a significant effect on the blood parameters of the born lambs.
Conclusions: In general, the use of chromium, especially in the form of chromium-methionine and chromium nanoparticles, is recommended during the transfer phase of sheep under the influence of heat stress.

Keywords

Main Subjects


Abdelnour, S. A., Abd El-Hack, M. E., Khafaga, A. F., Arif, M., Taha, A. E., & Noreldin, A. E. (2019). Stress biomarkers and proteomics alteration to thermal stress in ruminants: a review. Journal of Thermal Biology, 79, 120–134. doi: 10.1016/j.jtherbio.2018.12.013
Alfano, F. R. D. A., Palella, B. I., & Riccio, G. (2011). Thermal environment assessment reliability using temperature—humidity indices. Industrial Health49(1), 95-106.‏ doi: 10.2486/indhealth.MS1097
Al-Saiadi, M. Y., Al-Shaikh, M. A., Al-Mofarrej, S. I., Al-Showeimi, T. A., Mogawer, H. H., & Dirrar, A. (2004). Effect of chelated chromium supplementation on lactation performance and blood parameters of Holstein cows under heat stress. Animal Feed Science and Technology, 117, 223-233. doi: 10.1016/j.anifeedsci.2004.07.008
Amoikon, E. K., Fernandez, J. M., Southern, L. L., Thompson, Jr. D.  L. Ward, T. L., & Olcott, B. M. (1995). Effects of chromium tripicolinate on growth, glucose tolerance, insulin sensitivity, plasma metabolites, and growth hormone in pigs. Journal of Animal Science, 73, 1123-1130. doi: 10.2527/1995.7341123x
Asadi, M., Toghdori, A., Ghoorchi, T., & Hatami, M. (2023). Influence of organic manganese supplementation on performance, digestibility, milk yield and composition of Afshari ewes in the transition period, and the health of their lambs. Animal Production Research, 12(1), 1-12. doi: 10.22124/AR.2023.23808.1752 [In Persian]
Asadi, M., Toghdory, A., Ghoorchi, T., & Kargar, Sh. (2018). Effect of physical form of the concentrate and buffer type on the rumen and blood parameters and microbial protein synthesis in fattening Dalagh lamb. Animal Science Journal (Pajouhesh & Sazandegi), 122(1), 143-158. doi: 10.22092/asj.2018.121090.1658 [In Persian]
Bell, A. W, Greenwood, P. L., & Ehrhardt, R. A. (2005). Regulation of metabolism and growth during prenatal growth. In: Burrin DG, Mersmann HJ, editor. Biology of metabolism in growing animals. Edinburgh, UK: Elsevier Limited. doi: 10.1016/S1877-1823(09)70008-6
Besong, S., Jackson, J. A., Trammell, D. S., & Akay, V. (2001). Influence of supplemental chromium on concentrations of liver triglyceride, blood metabolites and rumen VFA profile in steers fed a moderately high fat diet. Journal of Dairy Science, 84, 1679-1685. doi: 10.3168/jds.S0022-0302(01)74603-6
Broderick, G. A., & Kang, J. H. (1980). Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. Journal of Dairy Science, 54, 1176-1183. doi: 10.3168/jds.S0022-0302(80)82888-8
Bunting, L. D., Tarifa, T. A., Crochet, B. T., Fernandez, J. M., Depew, C. L., & Lovejoy, J. C. (2000). Dietary inclusion of chromium propionate and (or) calcium propionate influences gastrointestinal development and insulin function in dairy calves. Journal of Dairy Science, 83, 2491-2498. doi: 10.3168/jds.S0022-0302(00)75141-1
Choi, S. J., Oh, J. M., & Choy, J. H. (2010). Biocompatible nanoparticles intercalated with anticancer drug for target delivery: pharmacokinetic and biodistribution study. Journal of Nanoscience and Nanotechnology10(4), 2913-2916.‏ doi: 10.1166/jnn.2010.1415
Cortas, N. K., & Wakid, N. W. (1990). Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clinical Chemistry, 36(8), 1440-1443. doi: 10.1093/clinchem/36.8.1440
Dallago, B., McManus, C., Caldeira, D., Lopes, A., Paim, T., Franco, E., Borges, B., Teles, P., Correa, P., & Louvandini, H. (2011). Performance and ruminal protozoa in lambs with chromium supplementation. Veterinary Science Research, 90, 253-256. doi: 10.1016/j.rvsc.2010.06.015
Dębski, B., Zalewski, W., Gralak, M. A., & Kosla, T. (2004). Chromium-yeast supplementation of chicken broilers in an industrial farming system. Journal of Trace Elements in Medicine and Biology 18(1), 47-51.‏ doi: 10.1016/j.jtemb.2004.02.003
Dehority, B. A., & Males, J. R. (1984). Rumen Fluid Osmolality: Evaluation of influence upon the occurrence and numbers of holotrich protozoa in sheep. Journal Animal Science, 38, 865-870. doi: 10.2527/jas1974.384865x
Deka, R. S., Mani, V., Kumar, M., Shiwajirao, Z. S., & Kaur, H. (2015). Chromium supplements in the feed for lactating Murrah buffaloes (Bubalus bubalis): influence on nutrient utilization, lactation performance, and metabolic responses. Biological Trace Element Research, 168, 362-371.‏ doi: 10.1007/s12011-015-0372-x
Domínguez-Vara, I. A., González-Muñoz, S. S., Pinos-Rodríguez, J. M., Bórquez-Gastelum, J. L., Bárcena-Gama, R., Mendoza-Martínez, G., Zapata, L. E., & Landois-Palencia, L .L. (2009). Effect of feeding selenium-yeast and chromium-yeast to finishing lambs on growth, carcass characteristics, and blood hormones and metabolites. Journal of Animal Feed Science and Technology, 152, 42-49. doi: 10.1016/j.anifeedsci.2009.03.008
Duffield, T. F., Merrill, J. K., & Bagg, R. N. (2012). Meta-analysis of the effects of monensin in beef cattle on feed efficiency, body weight gain, and dry matter intake. Journal of Animal Science90(12), 4583-4592.‏ doi: 10.2527/jas.2011-5018
 Emami, A., Zali, A. Ganjkhanlou, M., Hozhabri, A., & Akbari, A.  (2013). Effect of different levels of chromium methionin supplementation on growth performance, meat oxidative stability and ruminal metabolites of male goat kids. Iranian Journal of Applied Animal Science, 3(2), 273-278.
Forbes, C. D., Fernandez, J. M., Bunting, L. D., Southern, L. L., Thompson, D. L., Gentry, L. R., & Chapa, A. M. (1998). Growth and metabolic characteristics of Suffolk and Gulf Coast Native yearling ewes supplemented with chromium tripicolinate. Small Ruminant Research, 28(2), 149-160. doi: 10.1016/S0921-4488(97)00078-3
Ghorbani, A., Noorian Soroor, M. A., & Moini, M. M. (2017). The effect of zinc and selenium supplements on feed intake, digestibility and parameters of ruminal fermentation in sheep. Journal of Animal Science, 36, 11-17. doi: 10.22092/asj.2017.113262
Ghorbani, A., Sadri, H., Alizadeh, A. R., & Bruckmaier, R. M. (2012). Performance and metabolic responses of Holstein calves to supple-mental chromium in colostrum and milk. Journal of Dairy Science, 95, 5760-5769. doi: 10.3168/jds.2012-5500
Haldar, S., Mondal, S. Samanta, S., & Ghosh, T. K. (2009b). Performance traits and metabolic responses in goats (Capra hircus) supplemented with inorganic trivalent chromium. Journal of Biological Trace Element Research, 131, 110-123. doi: 10.1007/s12011-009-8356-3
Harrison, G. A., Hemken, R. W., Dawson, K. A., Harmon, R. J., & Barker, K. B. (1988). Influence of addition of yeast culture supplement to diets of lactating cows on ruminal fermentation and microbial populations 1. Journal of Dairy Science, 71, 2967-2975. doi: 10.3168/jds.S0022-0302(88)79894-X
Harvey, K. M., Cooke, R. F., & Marques, R. S. (2021). Supplementing trace minerals to beef cows during gestation to enhance productive and health responses of the offspring. Animals, 11(4), 1159. doi: 10.3390/ani11041159
Hassan, F. A, Mahmoud, R., & El-Araby, I. E. (2017). Growth performance, serum biochemical, economic evaluation and IL6 gene expression in growing rabbits fed diets supplemented with zinc nanoparticles. Zagazig Veterinary Journal45(3), 238-249.‏ doi: 10.21608/zvjz.2017.7949
Hill, E. K., & Li, J. (2017). Current and future prospects for nanotechnology in animal production. Journal of Animal Science and Biotechnology8(1), 1-13.‏ doi: 10.1186/s40104-017-0157-5
Hodgson, E., Cope, W. G., & Leidy, R. B. (2004). Classes of toxicants: use classes. Pp. 49-74 in Textbook of Modern Toxicology. E. A. Hodgson Ed. 3th Ed. Wiley-Interscience, New Jersey.  doi: 10.1002/0471646776.ch5
Ibrahim, W. M., Oda, S. S., & Khafaga, A. F. (2017). Pathological evaluation of the effect of zinc oxide nanoparticles on chromium-induced reproductive toxicity in male albino rats. Alexandria Journal of Veterinary Sciences, 53(2), 24-32. doi: 10.5455/ajvs.251315
Jin, D., Kang, K., Wang, H., Wang, Z., Xue, B., Wang, L., Xu, F., & Peng, Q. (2017). Effects of di-etary supplementation of active dried yeast on fecal methanogenic archaea diversity in dairy cows. Anaerobe Journal, 44, 78-86.  doi: 10.1016/j.anaerobe.2017.02.007
Kaneko, J. J. (2008). Clinical biochemistry of domestic animals. 6th ed. Academic Press, Inc., San Diego.
Kargar, S., Mousavi, F., & Karimi-Dehkordi, S. (2018). Effects of chromium supplementation on weight gain, feeding behaviour, health and metabolic criteria of environmentally heat-loaded Holstein dairy calves from birth to weaning. Archives of Animal Nutrition, 72, 443-457.  doi: 10.1080/1745039X.2018.1510157
Kargar, S., Mousavi, S., Karimi-Dehkordi, M., & Ghaffari, M. H, (2018). Growth performance, feeding behavior, health status, and blood metabolites of environmentally heat-loaded Holstein dairy calves fed diets supplemented with chromium. Journal of Dairy Science, 101, 1-12.  doi: 10.3168/jds.2017-14154
Kashfi, H., Yazdani, A. R., & Latifi, M. (2011). Economical study of effective management strategies on prevention of displaced abomasum in transition period in commercial dairy farms in Shahroud. Research on Animal Production, 2(4), 61-70.‏ doi: 10.1586/s40104-564-0877-5
Kegley, E. B., Galloway, D. L., & Fakler, T. M. (2000). Effect of dietary Chromium-L- methionine on glucose metabolism of beef steers. Journal of Animal Science, 78, 3177-3183.  doi: 10.2527/2000.78123177x
Kitchalong, L., Fernandez, J. M. Bunting, L. D. Southern, L. L., & Bidner, T. D. (1995). Influence of chromium tripicolinate on glucose metabolism and nutrient partitioning in growing lambs. Journal of Animal Science, 73, 2694-2705.  doi: 10.2527/1995.7392694x
Kojouri, G. A., & Shirazi, A. (2007). Serum concentrations of Cu, Zn, Fe, Mo and Co in newborn lambs following systemic administration of vitamin E and selenium to the pregnant ewes. Small Ruminant Research70(2-3), 136-139.‏  doi: 10.1016/j.smallrumres.2006.02.002
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.‏ doi: 10.1007/s12011-018-1310-5
Matthews, J. O., Southern, L. L., Fernandez, J. M., Pontif, J. E., Bidner, T. D., & Odgaard, R.L. (2001). Effect of chromium picolinate and chromium propionate on glucose and insulin kinetics of growing barrows and on growth and carcass traits of growingfinishing barrows. Journal of Animal Science, 79, 2172-2178.  doi: 10.2527/2001.7982172x
Maximino, N., Pérez-Alvarez, M., Sierra-Ávila, R., Ávila-Orta, C. A., Jiménez-Regalado, E., Bello, A. M., & Cadenas-Pliego, G. (2018). Oxidation of copper nanoparticles protected with different coatings and stored under ambient conditions. Journal of Nanomaterials, 2018, 512768. doi: 10.1155/2018/9512768
Mayorga, E. J., Kvidera, S. K., Seibert, J. T., Horst, E. A., Abuajamieh, M., Al-Qaisi, M., Lei, S., Ross, J. W., Johnson, C. D., Kremer, B., Ochoa, L., Rhoads, R. P., & Baumgard, L. H. (2019). Effects of dietary chromium propionate on growth performance, metabolism, and immune biomarkers in heat-stressedfinishing pigs1. Journal of Animal Science, 97, 1185-1197.  doi: 10.1093/jas/sky484
Meyer, A. M., Reed, J. J, Neville, L., Thorson, J., Maddock-Carlin, R., Taylor, B., Reynolds, P., Redmer, A., Luther, S., Hammer, J., Vonnahme, A., & Caton, S. (2011). Nutritional plane and selenium supply during gestation affect yield and nutrient composition of colostrum and milk in primiparous ewes. Journal of Animal Science, 89, 1627-1639.  doi: 10.2527/jas.2010-3394
Moezzi, A., McDonagh, A. M., & Cortie, M. B. (2012). Zinc oxide particles: Synthesis, properties and applications. Chemical Engineering Journal185, 1-22.‏  doi: 10.1016/j.cej.2012.01.076
Moreira, P. S. A., Palhari, C., & Berber, R. C. A. (2020). Dietary chromium and growth performance animals: a review. Scientific Electronic Archives, 13(7), 59-66.‏  doi: 10.36560/13620201151
Mosayebi, M., Aliarabi, H., & Farahavar, A. (2017). Effect of adding organic chromium and L-carnitine to feedlot lamb's diet on performance, glucose metabolism and some blood parameters. Journal of Ruminant Research, 5, 81-110.  doi: 10.29252/rap.10.23.65 [In Persian]
Mousaie, A., Valizadeh, R., Naserian, A.  A., Heidarpour, M., & Mehrjerdi, H. K. (2014). Impacts of feeding selenium-methionine and chromium-methionine on performance, serum components, antioxidant status, and physiological responses to transportation stress of Baluchi ewe lambs. Biological Trace Element Research162, 113-123.‏ doi: 10.1007/s12011-014-0162-x
Mousavi, F., Karimi-Dehkordi, S., Kargar, S., & Ghaffari, M. H. (2019). Effect of chromium supplementation on growth performance, meal pattern, metabolic and antioxidant status and insulin sensitivity of summer-exposed weaned dairy calves. Animal13(5), 968-974.  doi: 10.1017/S1751731118002318
Mousavi, F., Karimi-Dehkordi, S., Kargar, S., & Khosravi-Bakhtiari, M. (2019). Effects of dietary chromium supplementation on calf performance, metabolic hormones, oxidative status, and susceptibility to diarrhea and pneumonia. Animal Feed Science and Technology, 248, 95-105.  doi: 10.1016/j.anifeedsci.2019.01.004
Mullins, C. R., Mamedova, L. K., Brouk, M. J., Moore, C. E., Green, H. B., Perfield, K. L., & Bradford, B. J. (2012). Effects of monensin on metabolic parameters, feeding behavior, and productivity of transition dairy cows. Journal of Dairy Science95(3), 1323-1336.‏  doi: 10.3168/jds.2011-4744
National Research Council. (2001). Nutrient Requirements for Dairy Cattle. 7th Revised edition. National Academies Press, Washington, DC, USA.
National Research Council. (2007). Nutrient Requirements of Small Ruminants. Sheep, goats, cervide and new world camelids. Washington, DC: National Academy Press.
Nikkhah, A., Mirzaei, M., Khorvash, M., Rahmani, H. R., & Ghorbani, G. R. (2011). Chromium improves production and alters metabolism of early lactation cows in summer. Journal of Animal Physiology and Animal Nutrition, 95, 81-89.  doi: 10.1111/j.1439-0396.2010.01007.x
Nonaka, I., Takusari, N., Tajima, K., Suzuki, T., Higuchi, K., & Kurihara, M. (2008). Effects of high environmental temperatures on physiological and nutritional status of prepubertal Holstein heifers. Livestock Science, 113(1), 14-23.  doi: 10.1016/j.livsci.2007.02.010
Noori, G. H., Amanlou, R. H., Harakinejhad, M. T., Eskandainasab, M. P., & Mirzayee, H. R. (2015). The effects of chromium supplementation during late pregnancy on performance and blood metabolites of twin-bearing ewes. Journal of Ruminant Research, 3(1), 35-52.  doi: 10.2347/s15961-014-7642-x [In Persian]
Nooriyan Soroor, M. E., Haghi Ghobadi, M., Eskandari, K., & Moeini, M. M. (2018). Effects of three sources of chromium on growth traits, fermentation parameters, protozoa population and some blood metabolites in Mehraban male lambs. Animal Science Journal (Pajouhesh & Sazandegi), 123, 149-166. doi: 10.22092/asj.2018.121012.1654 [In Persian]
Ohh, S. J., & Lee, J. Y. (2005). Dietary chromium-methionine chelate supplementation and animal performance. Asian-Australasian Journal of Animal Sciences18(6), 898-907. doi: 10.5713/ajas.2005.898
‏ Ottenstein, D. M., & Batler, D. A. (1971). Imoroved gas chromatography separation of free acids C2-C5 in dilute solution. Analytical Chemistry, 43, 952-955.  doi: 10.1093/chromsci/9.11.673
Page, T. G., Southern, L. L., Ward, T. L., & Thompson, Jr D. L. (1993). Effect of chromium
picolinate on growth and serum and carcass traits of growing-finishing pigs. Journal of
Animal Science
, 71, 656-662.  doi: 10.2527/1993.713656x
Pantelić, M., Jovanović, L. J, Prodanović, R., Vujanac, I., Đurić, M., Ćulafić, T., & Kirovski, D. (2018). The impact of the chromium supplementation on insulin signalling pathway in different tissues and milk yield in dairy cows. Journal of Animal Physiology and Animal Nutrition102(1), 41-55.‏  doi: 10.1111/jpn.12655
Pechova, A., Podhorsky, A., Lokajova, E., Pavlata, L., & Illek, J. (2002). Metabolic effects of chromium supplementation in dairy cows in the peripartal period. Acta Veterianaria Brunensis, 71, 9-18. doi: 10.2754/avb200271010009
Phan, T. T. V., Huynh, T. C., Manivasagan, P., Mondal, S., & Oh, J. (2020). An up-to-date review on biomedical applications of palladium nanoparticles. Nanomaterials10(1), 66.‏  doi: 10.3390/nano10010066
Raje, K., Ojha, S., Mishra, A., Munde, V. K., Rawat, C., Chaudhary, S. K. (2018). Impact of supplementation of mineral nano particles on growth performance and health status of animals: A review. Journal of Entomology and Zoology Studies, 6, 1690-1694. doi: 10.21608/svu.2023.191602.1258
Rikhari, K., Tiwari, D., & Kumar, A. (2010). Effect of dietary supplemental chromium on nutrient utilization, rumen metabolites and enzyme activities in fistulated crossbred male cattle. Indian Journal of Animal Sciences, 80(Abstr). doi: 10.1007/s113022-014-0162-x
Robinson, J. J., McDonald, I., Fraser, C., & Crofts, R. M. J. (1977). Studies on reproduction in prolific ewes I. Growth of the products of conception. The Journal of Agricultural Science, 88(3), 539-552. doi: 10.1017/S0021859600046372
SAS Institute. (2004). User’s Guide. Version 9.1: Statistics. SAS Institute, Cary, NC.
Seifalinasab, A., Mousaie, A., Sattaei Mokhtari, M., & Doumari, H. (2019). The effect of organic chromium supplement on growth performance, nutrients digestibility and some ruminal fermentation parameters and blood metabolites in fattening lambs. Research on Animal Production, 10(23), 65-74. doi: 10.29252/rap.10.23.65 [In Persian]
Soltan, M. A. (2010). Effect of dietary chromium supplementation on productive and repro-ductive performance of early lactating dairy cows under heat stress. Journal of Animal Physiology and Animal Nutrition, 94, 264-272.  doi: 10.1111/j.1439-0396.2008.00913.x
Soltan, M. A., Almujalli, A. M., Mandour, M. A., & Abeer, M. E. S. (2012). Effect of dietary chromium performance, supplementation rumen on growth fermentation characteristics and some blood serum units of fattening dairy calves under heat stress. Pakistan Journal of Nutrition, 11(9), 751-756. doi: 10.22092/asj.2018.121012.1654
Soriani, N., Panella, G., & Calamari, L. (2013). Rumination time during the summer season and its relationships with metabolic conditions and milk production. Journal of Dairy Science, 96, 5082-5094. doi: 10.3168/jds.2013-6620
Spears, J. W. (2019). Boron, chromium, manganese, and nickel in agricultural animal production. Biological Trace Element Research188(1), 35-44. doi: 10.1007/s12011-018-1529-1‏
Stahlhut, H. S., Whisnant, C. S., Lloyd, K. E., Baird, E. J., Legleiter, L. R., Hansen, S. L., & Spears, J. W. (2006). Effect of chromium supplementation and copper status on glucose and lipid metabolism in Angus and Simmental beef cows. Animal Feed Science and Technology128(3-4), 253-265.‏ doi: 10.1016/j.anifeedsci.2005.11.002
Stewart, W. C., Bobe, G., Pirelli, G. J., Mosher, W. D., & Hall, J. A. (2012). Organic and inorganic selenium: III. Ewe and progeny performance. Journal of Animal Science, 90, 4536-4543.  doi: 10.2527/jas.2011-5019
Taheri, H. R., & Tavakoli Alamuti, M. (2011). Animal nutrition science. 1thed. Aeeizh publication, Tehran, Iran. P. 432. [In Persian]
Travan, A., Pelillo, C., Donati, I., Marsich, E., Benincasa, M., Scarpa, T., & Paoletti, S. (2009). Non-cytotoxic silver nanoparticle-polysaccharide nanocomposites with antimicrobial activity. Biomacromolecules, 10(6), 1429-1435.‏ doi: 10.1021/bm900039x
Uyanik, F. (2001). The effects of dietary chromium supplementation on some blood parameters in sheep. Journal of Biological Trace Element Research, 84, 93-101.  doi: 10.1385/BTER:84:1-3:093
Uyanik, F., Kaya, Ş., Kolsua, A. H., Eren, M., & Şahin, N. (2002). The effect of chromium supplementation on egg production, egg quality and some serum parameters in laying hens. Turkish Journal of Veterinary and Animal Sciences, 26(2), 379-387. doi: 10.5607/s12011-064-5862-x
Vincent, J. B. (2015). Is the pharmacological mode of action of chromium (III) as a second messenger. Biological Trace Element Research, 166, 7-12. doi: 10.1007/s12011-015-0231-9
Wang, C., Liu, Q., Yang, W. Z., Dong, Q., Yang, X. M., He, D. C., Zhang, P., Dong, K. H., & Huang, Y. X. (2009). Effects of selenium yeast on rumen fermentation, lactation performance and feed digestibilities in lactating dairy cows. Livestock Science, 126, 239-244.  doi: 10.1016/j.livsci.2009.07.005
Wang, M. Q., Xu, Z. R., Zha, L. Y., & Lindemann, M. D. (2007). Effects of chromium nanocomposite supplementation on blood metabolites, endocrine parameters and immune traits in finishing pigs. Animal Feed Science and Technology, 139, 69-80.  doi: 10.1016/j.anifeedsci.2006.12.004
West, J. W. (1999). Nutritional strategies for managing the heat-stressed dairy cows. Journal of Animal Science, 77, 21-29.  doi: 10.2527/1997.77suppl_221x
Yari, M., Baharifar, M., Alizadeh Masuleh, A., & Mousaie, A. (2018). Growth performance, feeding behavior and physiological responses of young growing Holstein male calves to dietary chromium-methionine (Cr-Met) supplementation related to body weight and age. Iranian Journal of Applied Animal Science8(3), 415-422.‏  doi: 10.1017/S0021859600046372
Yari, M., Nikkhah, A., Alikhani, M., Khorvash, M., Rahmani, H., & Ghorbani, G. R. (2010). Physiological calf responses to increased chromium supply in summer. Journal of Dairy Science, 93, 4111-4120. doi: 10.3168/jds.2009-2568
Zhao, M. D., Di, L. F., Tang, Z. Y., Jiang, W., & Li, C. Y. (2019). Effect of tannins and cellulase on growth performance, nutrients digestibility, blood profiles, intestinal morphology and carcass characteristics in Hu sheep. Asian-Australasian Journal of Animal Sciences, 32, 1540-1547.  doi: 10.5713/ajas.18.0901