Access to shade reduces DNA damage of Holstein cows under mild heat stress
A. S. de Abreu A , V. Fischer B E F , A. Thaler C , M. T. Stumpf D , F. Petronilho A , D. S. Florentino A , N. R. Hlavac A , M. Uczay C , E. Paludo C , P. H. E. Weiss C and C. I. G. Vogel C
+ Author Affiliations
- Author Affiliations
A UNISUL University, Avenida José Acácio Moreira, 787 – Dehon, Tubarão, SC 88704-900, Brazil.
B Department of Animal Science, Federal University of Rio Grande do Sul, Avenida Bento Gonçalves, 7712, Porto Alegre, CEP 91540-000, Brazil.
C Department of Animal and Food Production, Santa Catarina State University (UDESC), Avenida Luiz de Camões, 2090 – Conta Dinheiro, Lages, SC 88520000, Brazil.
D College of Agroecology, Federal University of Rio Grande, Avenida Marechal Floriano Peixoto, 2236, São Lourenço do Sul, RS 96170000, Brazil.
E Present address: Avenida Bento Gonçalves, 7712, Porto Alegre, Rio Grande do Sul, Brazil.
F Corresponding author. Email: vivinha.fischer@hotmail.com
Animal Production Science 60(12) 1539-1546 https://doi.org/10.1071/AN19075
Submitted: 8 February 2019 Accepted: 17 January 2020 Published: 29 April 2020
Abstract
Context: The effect of heat stress on the production and physiology of lactating dairy cows is well documented in literature. However, little is known about the effect of the provision of shade on DNA damage.
Aims: The present study aimed to evaluate the effects of shade provision on physiological, oxidative-stress, and DNA-strand damage in dairy cows exposed to mild heat stress.
Methods: The study was conducted at Lages, SC, Brazil, during 15 days in a southern hemisphere summer (January and February), with 14 lactating Holstein (n = 10) and Holstein × Jersey crossbreed (n = 4) dairy cows. Animals were randomly allocated to two groups of seven animals each (named as shaded and unshaded). These two groups were evaluated in the following three different periods: pre-stress period (5-day duration), stress period (4-day duration) and post-stress period (6-day duration). Shaded cows had free access to shade throughout the study; unshaded cows were prevented from accessing shade only in the stress period. Physiological (rectal temperature, heart and respiratory frequencies and panting score) and DNA-damage parameters (through Comet assay), as well as oxidative stress (in blood: carbonyl content, nitrite : nitrate ratio, thiobarbituric acid-reactive substances, TBARS) were evaluated.
Key results: In the stress period, shade deprivation resulted in higher values of respiratory rate, indicating that cows were under heat stress. In addition, DNA-damage levels were higher in this circumstance, probably due to inhibition of the DNA-repair systems by the thermal stress as well as thermal stress acting as a DNA-damage agent.
Conclusions: In a high-altitude subtropical region, during the hot season, shade provision decreases solar radiation heating effects and, thus, reduces DNA damage and the negative effects on cow metabolism and cell structure.
Implications: Shade effects on cow metabolism and cell structure must be taken into consideration in the planning of dairy farms and our results suggest that shade availability must not be disregarded, even in situations of mild heat stress.
Additional keywords: animal physiology, cell biology, climate, dairy cows, subtropical.
References
AOAC (Association of Official Analytical Chemists) (1995) ‘Official methods of analysis.’ 18th edn. (AOAC International: Arlington, VA)Baccari F, Jr (2001) ‘Manejo ambiental da vaca leiteira em climas quentes.’ 1st edn. (Universidade Estadual de Londrina: Londrina, PR)
Banks S, King SA, Irvine DS, Saunders PT (2005) Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 129, 505–514.
| Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 15798026PubMed |
Bernabucci B, Ronchi N, Lacetera N, Nardone A (2002) Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of Dairy Science 85, 2173–2179.
| Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season.Crossref | GoogleScholarGoogle Scholar |
Bernabucci B, Lacetera N, Baumgard LH, Nardone A (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4, 1167–1183.
| Metabolic and hormonal acclimation to heat stress in domesticated ruminants.Crossref | GoogleScholarGoogle Scholar |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Buege JA, Aust SA (1978) Microsomal lipid peroxidation. Methods in Enzymology 52, 302–310.
| Microsomal lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 672633PubMed |
Buffington DE, Collazo-Arrocho A, Canton GH, Pitt D, Thatcher WW, Collier RJ (1981) Black globe-humidity index (BGHI) as comfort equation for dairy cows. Transactions of the ASAE. American Society of Agricultural Engineers 24, 711–714.
| Black globe-humidity index (BGHI) as comfort equation for dairy cows.Crossref | GoogleScholarGoogle Scholar |
Celi P (2010) The role of oxidative stress in small ruminants’ health and production. Revista Brasileira de Zootecnia 39, 348–363.
| The role of oxidative stress in small ruminants’ health and production.Crossref | GoogleScholarGoogle Scholar |
da Silva RG, Guilhermino MM, de Morais DAEF (2010) Thermal radiation absorbed by dairy cows in pasture. International Journal of Biometeorology 54, 5–11.
| Thermal radiation absorbed by dairy cows in pasture.Crossref | GoogleScholarGoogle Scholar | 19543921PubMed |
Dalcin VC, Fischer V, Daltro DS, Alfonzo EPM, Stumpf MT, Kolling GJ, Da Silva MVGB, McManus C (2016) Physiological parameters for thermal stress in dairy cattle. Revista Brasileira de Zootecnia 45, 458–465.
| Physiological parameters for thermal stress in dairy cattle.Crossref | GoogleScholarGoogle Scholar |
Darzynkiewicz Z, Zhao H (2011) Detection of DNA strand breaks in apoptotic cells by flow- and image-cytometry. Methods in Molecular Biology 682, 91–101.
| Detection of DNA strand breaks in apoptotic cells by flow- and image-cytometry.Crossref | GoogleScholarGoogle Scholar | 21057923PubMed |
De Rensis F, Garcia-Ispierto I, López-Gatius F (2015) Seasonal heat stress: clinical implications and hormone treatments for the fertility of dairy cows. Theriogenology 84, 659–666.
| Seasonal heat stress: clinical implications and hormone treatments for the fertility of dairy cows.Crossref | GoogleScholarGoogle Scholar | 26025242PubMed |
Du Preez JH (2000) Parameters for the determination and evaluation of heat stress in dairy cattle in South Africa. The Onderstepoort Journal of Veterinary Research 67, 263–271.
Fournel S, Ouellet V, Charbonneau E (2017) Practices for alleviating heat stress of dairy cows in humid continental climates: a literature review. Animal
| Practices for alleviating heat stress of dairy cows in humid continental climates: a literature review.Crossref | GoogleScholarGoogle Scholar |
García O, Romero I, Gonzáles JE, Moreno DL, Cuétara E, Rivero Y, Gutiérrez A, Pérez CL, Álvarez A, Carnesolta D, Guevara I (2011) Visual estimation of the percentage of DNA in the tail of comet assay: evaluation of different approaches in an intercomparison exercise. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 720, 14–21.
| Visual estimation of the percentage of DNA in the tail of comet assay: evaluation of different approaches in an intercomparison exercise.Crossref | GoogleScholarGoogle Scholar |
Garcia AB, Angeli N, Machado L, Cardoso FC, Gonzalez F (2015) Relationships between heat stress and metabolic and milk parameters in dairy cows in southern Brazil. Tropical Animal Health and Production 47, 889–894.
| Relationships between heat stress and metabolic and milk parameters in dairy cows in southern Brazil.Crossref | GoogleScholarGoogle Scholar | 25851928PubMed |
González FHD, Silva SC (2006) ‘Introdução a bioquímica clínica veterinária.’ 1st edn. (Universidade Federal do Rio Grande do Sul: Porto Alegre, RS, Brazil)
Houston BJ, Nixon B, Martin JH, De Luliis GN, Trigg NA, Bromfield EG, McEwan KE, Aitken RJ (2018) Heat exposure induces oxidative stress and DNA damage in the male germ line Biology of Reproduction 98, 593–606.
| Heat exposure induces oxidative stress and DNA damage in the male germ lineCrossref | GoogleScholarGoogle Scholar | 29351587PubMed |
Johnson HD, Ragsdale AC, Berry IL, Shanklin MD (1962) ‘Effect of various temperature–humidity combinations on milk production of Holstein cattle.’ Research Bulletin. (Missouri Agricultural Experimental Station, University of Missouri, Columbia, MO, USA)
Kadzere CT, Murphy MR, Silanikove N, Maltz E (2002) Heat stress in lactating dairy cow: a review. Livestock Production Science 77, 59–91.
| Heat stress in lactating dairy cow: a review.Crossref | GoogleScholarGoogle Scholar |
Kaneko H, Igarashi K, Kataoka K, Miura M (2005) Heat shock induces phosphorylation of histone H2AX in mammalian cells. Biochemical and Biophysical Research Communications 328, 1101–1106.
| Heat shock induces phosphorylation of histone H2AX in mammalian cells.Crossref | GoogleScholarGoogle Scholar | 15707990PubMed |
Kantidze OL, Velichko AK, Luzhin AV, Razin SV (2016) Heat-stress induced DNA damage. 8, 75–78.
| Heat-stress induced DNA damage.Crossref | GoogleScholarGoogle Scholar | 27437141PubMed |
Köppen W (1931). ‘Climatologia.’ 1st edn. (Fundo da Cultura Econômica: Buenos Aires, Argentina)
Liu F, Ruyter EM, Athorn RZ, Brewster CJ, Henman DJ, Morrison RS, Smits RJ, Cottrell JJ, Dunshea FR (2019) Effects of L-citrulline supplementation on heat stress physiology, lactating performance and subsequent reproductive performance of sows in summer. Journal of Animal Physiology and Animal Nutrition 103, 251–257.
| Effects of L-citrulline supplementation on heat stress physiology, lactating performance and subsequent reproductive performance of sows in summer.Crossref | GoogleScholarGoogle Scholar | 30485568PubMed |
Lubawy J, Daburon V, Chowański S, Słocińska M, Colinet H (2019) Thermal stress causes DNA damage and mortality in a tropical insect. The Journal of Experimental Biology.
| Thermal stress causes DNA damage and mortality in a tropical insect.Crossref | GoogleScholarGoogle Scholar | 31672731PubMed |
Mader TL, Davis MS, Brown-Brandl T (2006) Environmental factors influencing heat stress in feedlot cattle. Journal of Animal Science 84, 712–719.
| Environmental factors influencing heat stress in feedlot cattle.Crossref | GoogleScholarGoogle Scholar | 16478964PubMed |
National Research Council (2001) ‘Nutrient requirements of dairy cattle.’ (National Academic Press: Washington, DC)
Olive PL, Banáth JP, Durand RE (1990) Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the ‘comet’ assay. Radiation Research 122, 86–94.
| Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the ‘comet’ assay.Crossref | GoogleScholarGoogle Scholar | 2320728PubMed |
Perissinotto M, Moura DJ, Cruz VF, Souza SRL, Lima KAO, Mendes AS (2009) Thermal comfort on Subtropical and Mediterranean climate analyzing some physiological data through fuzzy theory. Ciência Rural 39, 1492–1498.
| Thermal comfort on Subtropical and Mediterranean climate analyzing some physiological data through fuzzy theory.Crossref | GoogleScholarGoogle Scholar |
Petrova NV, Velichko AK, Razin SV, Kantidze OL (2016) Early S-phase cell hypersensitivity to heat stress. Cell Cycle 15, 337–344.
| Early S-phase cell hypersensitivity to heat stress.Crossref | GoogleScholarGoogle Scholar | 26689112PubMed |
Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6, 707–728.
| Adaptation to hot climate and strategies to alleviate heat stress in livestock production.Crossref | GoogleScholarGoogle Scholar | 22558920PubMed |
Robertson JP, Van Soest PJ (1981) The detergent system of analysis and its application to human foods. In ‘The analysis of dietary fibre in foods’. (Eds WPT James, O Theander) pp. 123–158. (Marcel Dekker, New York, NY, USA)
Schütz KE, Rogers AR, Poulouin YA, Cox NR, Tucker CB (2010) The amount of shade influences the behavior and physiology of dairy cattle. Journal of Dairy Science 93, 125–133.
| The amount of shade influences the behavior and physiology of dairy cattle.Crossref | GoogleScholarGoogle Scholar | 20059911PubMed |
Schütz KE, Rogers AR, Cox NR, Webster JR, Tucker CB (2011) Dairy cattle prefer shade over sprinklers: effects on behavior and physiology. Journal of Dairy Science 94, 273–283.
| Dairy cattle prefer shade over sprinklers: effects on behavior and physiology.Crossref | GoogleScholarGoogle Scholar | 21183037PubMed |
Schütz KE, Cox NR, Tucker CB (2014) A field study of the behavioral and physiological effects of varying amounts of shade for lactating cows at pasture. Journal of Dairy Science 97, 3599–3605.
| A field study of the behavioral and physiological effects of varying amounts of shade for lactating cows at pasture.Crossref | GoogleScholarGoogle Scholar | 24731637PubMed |
Silanikove N (2000) Effects of heat stress on the welfare of extensively managed domestic ruminants. Livestock Production Science 67, 1–18.
| Effects of heat stress on the welfare of extensively managed domestic ruminants.Crossref | GoogleScholarGoogle Scholar |
Silanikove N, Shapiro F, Shinder D (2009) Acute heat stress brings down milk secretion in dairy cows by up-regulating the activity of the milk-borne negative feedback regulatory system. Biomed Central Physiology 9, 13–22.
Silva DC, Passini R (2017) Physiological responses of dairy cows as a function of environment in holding pen. Engenharia Agrícola 37, 206–214.
| Physiological responses of dairy cows as a function of environment in holding pen.Crossref | GoogleScholarGoogle Scholar |
Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175, 184–191.
| A simple technique for quantitation of low levels of DNA damage in individual cells.Crossref | GoogleScholarGoogle Scholar | 3345800PubMed |
Slimen IB, Najar T, Ghram A, Dabbebi H, Mrad MB, Abdrabbah M (2014) Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. International Journal of Hyperthermia 30, 513–523.
| Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review.Crossref | GoogleScholarGoogle Scholar | 25354680PubMed |
Stober M (1993) Identificação, anamnese, regiões básicas da técnica do exame clínico. In ‘Exame clínico dos bovinos’. 3rd edn. (Ed. M Rosemberg). p. 419. (Guanabara Koogan: Rio de Janeiro, Brazil)
Trout JP, Mcdowell LR, Hansen PJ (1998) Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress. Journal of Dairy Science 81, 1244–1250.
| Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress.Crossref | GoogleScholarGoogle Scholar | 9621225PubMed |
Tucker CB, Rogers AR, Schutz KE (2008) Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasture-based system. Applied Animal Behaviour Science 109, 141–154.
| Effect of solar radiation on dairy cattle behaviour, use of shade and body temperature in a pasture-based system.Crossref | GoogleScholarGoogle Scholar |
Van Iaer E, Tuyttens FAM, Ampe B, Sonck B, Moons CPH, Vandaele L (2015) Effect of summer conditions and shade on the production and metabolism of Holstein dairy cows on pasture in temperate climate. Animal 9, 1547–1558.
| Effect of summer conditions and shade on the production and metabolism of Holstein dairy cows on pasture in temperate climate.Crossref | GoogleScholarGoogle Scholar |
van Zelst SJ, Zupp L, Hayman DL, Setchell BP (1995) X–Y chromosome dissociation in mice and rats exposed to increased testicular or environmental temperatures. Reproduction, Fertility and Development 7, 1117–1121.
| X–Y chromosome dissociation in mice and rats exposed to increased testicular or environmental temperatures.Crossref | GoogleScholarGoogle Scholar |
Veissier I, Van Iaer E, Palme R, Moons CPH, Ampe B, Sonck B, Andanson S, Tuyttens FAM (2018) Heat stress in cows at pasture and benefit of shade in a temperate climate region. International Journal of Biometeorology 62, 585–595.
| Heat stress in cows at pasture and benefit of shade in a temperate climate region.Crossref | GoogleScholarGoogle Scholar | 29150763PubMed |
Vizzotto EF, Fischer V, Thaler Neto A, Abreu AS, Stumpf MT, Werncke D, Schmidt FA, McManus CM (2015) Access to shade changes behavioral and physiological attributes of dairy cows during the hot season in the subtropics. Animal 9, 1559–1566.
| Access to shade changes behavioral and physiological attributes of dairy cows during the hot season in the subtropics.Crossref | GoogleScholarGoogle Scholar | 25994200PubMed |
Žunić GO, Čolić M, Vučeljić M (2009) Nitrite to nitrate molar ratio is inversely proportional to oxidative cell damages and granulocytic apoptosis at the wound site following cutaneous injury in rats. Nitric Oxide 20, 264–269.
| Nitrite to nitrate molar ratio is inversely proportional to oxidative cell damages and granulocytic apoptosis at the wound site following cutaneous injury in rats.Crossref | GoogleScholarGoogle Scholar |
