SciELO - Scientific Electronic Library Online

 
vol.31 issue4PROCESO EDITORIAL (Séptima entrega): Responsabilidades de los autores (1era. parte)Sources of bias in genetic association studies in cattle: A review author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Revista Colombiana de Ciencias Pecuarias

Print version ISSN 0120-0690

Rev Colom Cienc Pecua vol.31 no.4 Medellín Oct./Dec. 2018

https://doi.org/10.17533/udea.rccp.v31n4a01 

Literature Review

Antioxidant supplementation in female ruminants during the periconceptional period: A review¤

Suplementación con antioxidantes en hembras rumiantes durante el periodo periconcepcional Revisión de literatura

Suplementação de antioxidantes em fêmeas de ruminantes durante o período periconcepcional Revisão de literatura

Juan Gonzalez-Maldonado 1   *  

José A Martínez-Aispuro 2  

Raymundo Rangel-Santos 1  

Raymundo Rodríguez-de Lara 1  

1Posgrado en Producción Animal, Departamento de Zootecnia, Universidad Autónoma Chapingo, Chapingo, Estado de México, México.

2Programa de Ganadería, Colegio de Postgraduados, Estado de México, México


Abstract

Oxidative stress is the result of an imbalance between free radicals and antioxidants. Under normal physiological conditions, free radicals are involved in reproductive events such as cell cycle activation, ovulation and luteolysis. However, when an overproduction of free radicals surpasses antioxidant capacity, oxidative damage, reproductive anomalies and diminished fertility occur. Supplementation with antioxidants prevents oxidative damage and can be incorporated into reproductive management to improve fertility in females. Selection of the preovulatory follicle, ovulation, fertilization, embryo development and formation of the corpus luteum occur during the periconceptional period. This is a dynamic period and the events are susceptible to oxidative stress damage. Therefore, the objective of this review is to discuss the effect of oxidative stress on reproductive events during the periconceptional period, as well as to address antioxidant supplementation during this period.

Key words: embryo; fertility; free radicals; oocytes; ovulation; oxidative stress

Resumen

El estrés oxidativo es generado por un desbalance entre radicales libres y antioxidantes. Bajo condiciones fisiológicas normales, los radicales libres participan en eventos reproductivos tales como activación del ciclo celular, ovulación y luteólisis. Sin embargo, cuando estos son producidos en cantidades que sobrepasan la capacidad antioxidante del organismo producen daño oxidativo y trastornos reproductivos que disminuyen la fertilidad de la hembra. La suplementación con antioxidantes previene el daño oxidativo y su incorporación a programas de manejo reproductivo puede ser una opción para mejorar la fertilidad de la hembra. La selección del folículo preovulatorio, ovulación, fecundación, desarrollo embrionario y formación del cuerpo lúteo ocurren durante el periodo periconcepcional. Este es un periodo dinámico y los eventos que ocurren en él son susceptibles a daño por estrés oxidativo. Por tanto, el objetivo de esta revisión es discutir el efecto del estrés oxidativo en los eventos reproductivos durante el periodo periconcepcional, así como la suplementación de antioxidantes en rumiantes durante este periodo.

Palabras clave: embrión; estrés oxidativo; fertilidad; ovocito; ovulación; radicales libres

Resumo

O stress oxidativo é gerado por um desequilíbrio entre radicais livres e antioxidantes. Sob condições fisiológicas normais, os radicais livres participam de eventos reprodutivos, como ativação do ciclo estral, ovulação e luteólise. No entanto, quando é produzido em quantidades que excedem a capacidade antioxidante do organismo, produzem danos oxidativos e distúrbios reprodutivos que diminuem a fertilidade da fêmea. A suplementação com antioxidantes previne o dano oxidativo e sua incorporação em programas de gerenciamento reprodutivo pode ser uma opção para melhorar a fertilidade da fêmea. A seleção do folículo pré-ovulatório, ovulação, fecundação, desenvolvimento embrionário e formação do corpo lúteo ocorrem durante o período periconcepcional. Este é um período dinâmico e os eventos que ocorrem são suscetíveis ao dano por estresse oxidativo. Portanto, o objetivo dessa revisão é fornecer ao leitor conhecimento sobre o efeito do estresse oxidativo em eventos reprodutivos durante o período periconcepcional, e também discutir a suplementação com antioxidantes em ruminantes durante este período.

Palavras-chave: embrião; estresse oxidativo; fertilidade; ovócito; ovulação; radicais livres

Introduction

Oxidative stress is defined as an imbalance between free radicals and antioxidants, caused by an increased production of the former or decreased concentrations of the latter (Halliwell and Whiteman, 2004). A free radical is a highly reactive atom or molecule that contains one or more unpaired electrons in its outer orbit, and extracts an electron from other compound to gain stability (Phaniendra et al., 2015). Reactive oxygen species (ROS), and reactive nitrogen species are the main types of free radicals (Agarwal et al., 2005). They are normally produced in the mitochondria, peroxisomes, during inflammation and phagocytosis (Lobo et al., 2010). Free radicals participate in diverse physiological processes without causing harm, but high concentrations can cause oxidative stress and damage to lipids, proteins and DNA (Silva and Coutinho, 2010). In farm animals, heat stress, dietary imbalances and bacterial infections can increase free radical production and oxidative stress (Celi and Gabai, 2015).

Antioxidants prevent or inhibit oxidation of the substrate (lipids, protein or DNA) by donating electrons (Halliwell and Gutteridge, 1995). Antioxidants can be classified as enzymatic and non-enzymatic. Enzymatic antioxidants include superoxide dismutase, catalase, glutathione peroxidase and glutathione oxidase, while the non-enzymatic group includes vitamins A, C and E, beta-carotene, and trace elements such as copper, manganese, selenium and zinc, which are cofactors of antioxidant enzymes (Leung, 1998; Agarwal et al., 2012; Pisoschi and Pop, 2015).

Free radicals are normally involved in reproductive events such as follicular development, ovulation, corpus luteum development, luteolysis and early embryo development (Rizzo et al., 2012). However, an imbalance between free radicals and antioxidants can cause failure to conceive. Reactive oxygen species are part of the mechanism controlling ovulation; failure to achieve enough intra-follicular concentrations to produce preovulatory follicle rupture causes follicular cyst in cattle (Rizzo et al., 2009; Talukder et al., 2014a). Talukder et al. (2015) reported that cows with ovulatory oestrous cycles have greater concentrations of superoxide dismutase and lower oxidative damage to lipid products than cows that did not ovulate. In addition, repeat breeder cows that fail to conceive after artificial insemination have higher serum concentrations of oxidative stress markers than pregnant cows (Rizzo et al., 2007). In this regard, Celi (2011) mentions that oxidative stress indicators are higher in cows experiencing late embryo mortality. In buffalos, blood concentrations of antioxidants vitamin E and β-carotene were lower and intra-follicular concentrations of ROS were higher in animals in anestrus than those with normal oestrous cycles (Kahlon and Singh, 2004; Jan et al., 2014).

Oxidative stress occurs during different periods in animal systems, and antioxidants can be supplemented to improve reproductive performance (Nayyar and Jindal, 2010). In this review, we are focused on the periconceptional period; which comprises the events preceding, during and immediately occurring after conception (Louis et al., 2008). These events include follicle wave emergence, preovulatory follicle selection, ovulation, fecundation, early embryo development and corpus luteum formation. Restriction to these events is because available hormone treatments allow controlling these events, and the time of occurrence can be predicted (Lucy et al., 2004; Rahman et al., 2008; Menchaca et al., 2017). Therefore, if oxidative stress is suspected during the occurrence of events in this period, antioxidants can be supplemented to specifically protect/improve such events. The objective of this review is to provide evidence of the impacts of oxidative stress during the periconceptional period. In addition, the effect of antioxidant supplementation during hormonal treatments in female ruminants will be addressed.

Effects of oxidative stress on preovulatory follicle development and oocyte competence

Follicles undergo primordial, primary, small preantral, large preantral and small antral stages before reaching the preovulatory stage (Braw-Tal and Yossefi, 1997). Mammalian females are born with a fixed number of primordial follicles from which a preovulatory follicle will be recruited. There are two types of follicular recruitment: initial and cyclic. Initial recruitment is a continuous process in primordial follicles that occurs before puberty, while cyclic recruitment starts after puberty under the control of increased gonadotropin production (McGee and Hsueh, 2000). After puberty, antral follicles are recruited in a predictable wave fashion between estruses (Adams et al., 2008). The follicle wave is preceded by a FSH surge, which allows cyclic antral follicle recruitment (Fortune et al., 2001). After recruitment takes place, selection and growth of the dominant follicle occurs under the influence of LH until the ovulatory stage occurs (Ginther, 2000). For a follicle to accomplish the dominant status, it must be capable of performing three fundamental tasks: expressing gonadotropin receptors, performing steroidogenesis, and having access to IGF-I (Quirk et al., 2004). Under conditions of declining progesterone production, such as luteolysis, the dominant follicle will reach the ovulatory stage. The time required for a primordial follicle to reach the ovulatory stage is at least 80 days (Britt, 2008). During this period, the follicle and its enclosed oocyte are exposed to harmful conditions such as oxidative stress.

The oocyte from the primordial follicle to the preovulatory stage is arrested at the diplotene stage of prophase I. The preovulatory surge of LH breaks diplotene arrest by reducing the intra- oocyte concentration of cyclic 3′,5′-adenosine monophosphate (cAMP) (Tripathy et al., 2010), which is associated with a rise in the intra-oocyte concentration of hydrogen peroxide (H2O2) (Pandey and Chaube, 2014). The intra-oocyte generation of a tonic level of H2O2 is necessary to exit diplotene stage arrest, but high concentrations of H2O2 produce oocyte apoptosis (Chaube et al., 2005; Tripathi et al., 2009). The H2O2 is part of the ROS family. It is generated after the dismutation of superoxide radical by superoxide dismutase and can then be scavenged by glutathione peroxidase or catalase (Valko et al., 2007). Potential intra-follicular sources of reactive oxygen species include steroidogenesis (Hanukoglu et al., 1993), leukocytes (Brännström and Enskog, 2002) and ATP generation by mitochondrial electron transport (Kala et al., 2016). In addition, the preovulatory peak of LH induces an increase in ROS production (Yacobi et al., 2007), which is necessary to accomplish ovulation (Shkolnik et al., 2011).

Embryo implantation is reduced when the oocyte comes from a follicle with a high percentage of granulosa cells producing ROS (Jancar et al., 2007). Apoptosis, induced by oxidative stress to granulosa cells (Shen et al., 2012), implies a reduction in nutrient supply and signal molecules to the oocyte (Kidder and Vanderhyden, 2010), which can disrupt oocyte meiotic maturation (Ratchford et al., 2008). Additionally, ROS causes DNA fragmentation, cell cycle arrest, and apoptosis (Chaube et al., 2005; Prasad et al., 2016). Thus, on one hand, a moderate increase in ROS production is used as a signal to break cell cycle arrest, but on the other, high concentrations disrupt oocyte quality. It is likely that the required amount of ROS within the follicle and oocyte is regulated, at least in part, by the intra-follicular antioxidant system.

The presence of antioxidants such as catalase, glutation peroxidase, superoxide dismutase, ascorbic acid, vitamin E, and β-carotene has been demonstrated in ruminant follicle compartments (Schweigert and Zucker, 1988; Behl and Pandey, 2002; Combelles et al., 2010; Gupta et al., 2011; Hennet et al., 2013; Hozyen et al., 2014). Antioxidants prevent oxidative damage by preventing ROS concentrations from reaching levels that could harm the follicle and oocyte. However, situations leading to increased ROS production or to a reduction in antioxidant concentrations are likely to affect fertility by causing oxidative damage. Examples of these situations are mastitis, negative energy balance and heat stress.

Mastitis causes a 26 to 28% reduction in conception rates when it occurs within 10 days before or 30 days after artificial insemination (Lavon et al., 2011). The reduced pregnancy rate after mammary gland infection can be explained by alterations in ovarian steroid production and gonadotropin secretion (Wolfenson et al., 2015). In addition, mastitis produces an imbalance between antioxidants and oxidants, leading to oxidative stress (Sharma et al., 2016; Shahid et al., 2017). Recently, it was found that cytoplasmic maturation and embryo viability is compromised when oocytes are cultured with follicular fluid from cows with mastitis (Roth et al., 2015). Mastitis is experimentally induced by injection of gram negative toxins, such as lipopolysaccharides (Asaf et al., 2014). Lipopolysaccharides disrupt follicular steroidogenesis by reducing the expression of gonadotropin receptors and steroidogenic enzymes (Magata et al., 2014), inducing apoptosis and oxidative stress in oocytes (Zhao et al. 2017). Moreover, mastitis decreases antioxidant blood concentrations and increases oxidant capacity in milk (Kizil et al. 2007; Atakisi et al., 2010). Thus, oxidant/antioxidant balance is compromised during mastitis infection.

The increase in milk production after parturition demands a great amount of nutrients, but the inability to consume the required quantity produces a negative energy balance. Thus, the body removes nutrients from internal reserves to sustain vital functions and milk production. The state of negative energy balance is characterized by weight loss, increase in blood concentrations of non-esterified fatty acids (NEFA) and ketone bodies such as beta-hydroxybutyrate (Adewuyi et al., 2005).

Negative energy balance can last for 10-12 weeks after calving, during which fertility is compromised (Butler, 2003). After analyzing the NEFA profile and β-hydroxybutyrate in blood serum and follicular fluid of cows after parturition (Leroy et al., 2004), Leroy et al. (2005; 2006) found that administration of these two metabolites to the culture medium reduces oocyte competence. Moreover, Van Hoeck et al. (2013) reported that oocyte redox status is affected by NEFA, suggesting that oxidative stress induced by NEFA is responsible for lowering oocyte competence in dairy cattle undergoing negative energy balance. In this regard, Song et al. (2014; 2016) reported that NEFAand β-hydroxybutyrate cause hepatocyte apoptosis by means of oxidative stress. In addition, cows showing signs of negative energy balance -such as body weight lost, increased concentrations of NEFA and β-hydroxybutyrate- suffer oxidative stress (Bernabucci et al., 2005; Pedernera et al., 2010), which can be explained by diminished blood and follicular concentrations of antioxidants such as β-carotene, vitamins C and E, superoxide dismutase, and glutathione peroxidase (Cigliano et al., 2014; De Bie et al., 2016).

Oxidative stress induced by heat stress disrupts fertility in dairy cattle (Roth, 2015). Heat stress increases ROS production and reduces the proportion of oocytes that attain nuclear maturation and the blastocyst formation rate (Nabenishi et al., 2012). In addition, Takahashi (2012) suggests that oxidative stress induced by high temperatures creates adverse intraoviductal conditions for oocytes, sperm and embryo. Even though antioxidant supplementation seems to be a feasible way of ameliorating the negative effect of heat stress in fertility (Hansen, 2013), De Rensis et al. (2017) concluded that more research is needed to identify an antioxidant regimen that can effectively protect oocytes from heat stress.

Effects of oxidative stress on sperm, corpus luteum development and embryo viability

Fertilization of the ovulated oocyte, formation of the corpus luteum and embryo cleavage occur after ovulation. As with the oocyte, reactive oxygen species are necessary for the sperm to achieve capacitation, but high concentrations are detrimental (Aitken et al., 2012). Sources of ROS in the sperm include mitochondria, cytosolic L-amino acid oxidases, and plasma membrane nicotinamide adenine dinucleotide phosphate oxidases (Aitken, 2017). Infertile men have been found to have higher concentrations of reactive oxygen species, lower concentrations of vitamin E, and lower total antioxidant capacity than fertile men (Benedetti et al., 2012). In cattle, oxidative stress induced by heat stress reduces the fertilization rate in dairy cattle during summer season relative to winter (Sartori et al., 2002).

An antioxidant system supports corpus luteum functionality. Luteal superoxide dismutase and vitamin C concentrations increase as the corpus luteum develops (Luck and Zhao, 1993; Vu et al., 2013), and an increase in luteal antioxidant activity has been reported during pregnancy (Al-Gubory et al., 2004). An antioxidant system is necessary to counteract the ROS generated by steroidogenic cells and mononuclear phagocytes (Kato et al., 1997), or by the inner environment of the corpus luteum. This is relevant since the mechanism used by PGF2α during luteolytic events implies the production of ROS and a decrease in antioxidant activity (Hayashi et al., 2003; Vu et al., 2012; Vu et al., 2013), resulting in low progesterone production.

A changing antioxidant status is detectable throughout the estrous cycle. According to Aydilek et al. (2014), total antioxidant activity is lower in the luteal than in the follicular phase of the estrus cycle in cows. Repeat breeder cows have higher concentrations of ROS during the crucial period of corpus luteum survival (days 12 and 16 of the estrous cycle), causing failure to conceive (Rizzo et al., 2007). However, a failure to generate enough ROS after induced luteolysis by PGF2α results in anovulation (Talukder et al., 2014b). This suggests that increased antioxidant activity during the luteal phase may be detrimental to reproductive performance in empty cows, but not for pregnant cows.

Oxidative stress is detrimental to embryo survival either by blocking progesterone supply or by a direct effect on embryo cells. The source of reactive oxygen species may come from metabolic activity of the embryo itself (Gupta et al., 2006) or from the maternal environment (Poston et al., 2011). Regarding the latter, it is known that maternal heat stress is responsible for induced embryonic death by increasing ROS production and antioxidant depletion, but not by heat stress itself (Ozawa et al., 2002). When ROS become uncontrolled, they cause morphological and functional alterations, which may block embryo development or apoptosis (Guérin et al., 2001), supporting the suggested implication of ROS in bovine embryo mortality (Celi et al., 2011).

The early embryo may be capable of developing some degree of resistance to the adverse effects of ROS as it grows. Ealy et al. (1993) reported that Holstein cow embryos become less susceptible to maternal heat stress after one day of pregnancy. Similarly, Morales et al. (1999) reported that nine- to 16 cell- embryos are more resistant to ROS insults than zygotes and blastocysts. Bain et al. (2011) suggested that susceptibility of the bovine embryo to ROS increases during the first 72 hours of embryonic life. In addition, differences in ROS resistance related to embryo sex have been reported (Pérez-Crespo et al., 2005); female embryos are more resistant than male embryos. These findings suggest that severity of ROS-induced embryo damage is developmental and sex dependent.

Antioxidant supplementation during the periconceptional period in female ruminants

Oocyte and embryo well-being can be compromised by oxidative damage generated as the result of common reproductive practices around the periconceptional period. Rectal palpation and artificial insemination are stressful to dairy cattle (Nakao et al., 1994) and cause oxidative stress (Cingi et al., 2012). These practices are commonly and repeatedly performed during estrus synchronization. A common practice among reproductive technicians, before artificial insemination, is to stimulate the reproductive tract via rectal massage for visualization of cervical mucus in order to reveal any infection. However, unexperienced technicians may cause rectal irritation, evidenced by the presence of blood on the palpating hand. This situation is also observed after multiple, prolonged or rough palpations, but it is unknown how much this can affect fertility.

Estrus synchronizations using progesterone- releasing devices is common in small ruminants and cattle. Several studies have reported inflammatory responses and changes in normal flora and vaginal histology of ewes and cattle after using estrus synchronization devices (Manes et al., 2010; Suárez et al., 2006; Walsh et al., 2007; Manes et al., 2015). In addition, Sönmez et al. (2009) reported a steady increase in ROS after intravaginal sponge insertion in goats, suggesting that sponge insertion can cause oxidative stress. The inflammatory response and oxidative stress induced by insertion of progesterone release devices may be responsible for the reduced fertility in ewes carrying intravaginal sponges (Manes et al., 2014).

Ovarian superstimulation of small and large ruminants is used to increase the number of oocytes and embryos that a female would normally produce during a normal estrous cycle. However, superstimulation is known to upregulate genes related to oxidative stress in cattle (Dias et al., 2013). In mice, an increase in oxidative damage in the uterus and oviduct (Park et al., 2015), as well as a reduction in oocyte mitochondria number and function, have been reported after single and repeated superstimulation. In addition, low quality oocytes -resulting in embryos with mitochondrial functional defects, which are more susceptible to oxidative damage- have been found during superstimulation (Komatsu et al., 2014). Since an oxidative insult is present during superstimulation, antioxidant supplementation may help to overcome some of the detrimental effects on oocyte and embryo quality. According to Liu et al. (2013) and Ben-Meir et al. (2015), antioxidant supplementation not only counteracts oxidative damage in the oocyte but also restores mitochondrial function.

The evidence suggests that antioxidant supplementation may be beneficial, by improving fertility during the periconceptional period. Evidence validating the effectiveness of antioxidant supplementation during hormonal treatment in ruminant females around this period is shown in Table 1. Parenteral antioxidant supplementation is probably the best option during the periconceptional period. As shown in Table 1, antioxidants were given via injection in all cases, probably because high concentrations in blood and other body compartments can be reached faster than through feed supplementation. In the case of vitamin E, for example, parenteral supplementation is a more effective way to improve antioxidant status in the short term compared with in-feed supplementation (Bourne et al., 2007; Mokhber-Dezfouli et al., 2008). This is relevant because a rapid effect is desired.

Table 1 Effect of antioxidant injection during the periconceptional period on ruminant fertility. 

In conclusion, free radicals participate in reproductive events occurring during the periconceptional period. However, situations leading to overproduction that surpasses antioxidant capacity cause oxidative stress and compromise fertility. Antioxidant supplementation during hormonal treatments carried out during this period can improve fertility in female ruminants.

References

Adewuyi AA, Gruys E, van Eerdenburg FJ. Non esterified fatty acids (NEFA) in dairy cattle. A review. Vet Q 2005; 27:117-126. [ Links ]

Adams GP, Jaiswal R, Singh J, Malhi P. Progress in understanding ovarian follicular dynamics in cattle. Theriogenology 2008; 69:72-80. [ Links ]

Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005; 3:28. [ Links ]

Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 2012; 10:49. [ Links ]

Aitken RJ, Jones KT, Robertson SA. Reactive oxygen species and sperm function--in sickness and in health. J Androl 2012; 33:1096-1106. [ Links ]

Aitken RJ. Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol Reprod Dev 2017. [ Links ]

Al-Gubory KH, Bolifraud P, Germain G, Nicole A, Ceballos-Picot I. Antioxidant enzymatic defence systems in sheep corpus lu- teum throughout pregnancy. Reproduction 2004; 128:767-774. [ Links ]

Asaf S, Leitner G, Furman O, Lavon Y, Kalo D, Wolfenson D, Roth Z. Effects of Escherichia coli- and Staphylococcus aureus- induced mastitis in lactating cows on oocyte developmental competence. Reproduction 2014; 147:33-43. [ Links ]

Atakisi O, Oral H, Atakisi E, Merhan O, Metin Pancarci S, Ozcan A, Marasli S, Polat B, Colak A, Kaya S. Subclinical mastitis causes alterations in nitric oxide, total oxidant and antioxidant capacity in cow milk. Res Vet Sci 2010; 89:10-13. [ Links ]

Aydilek N, Varişli Ö, Selek Ş, Korkmaz Ö, Atli MO, Taşkin A. The effect of estrous cycle on oxidant and antioxidant parameters in dairy cows. Kafkas Univ Vet Fak Derg 2014; 20:703-709. [ Links ]

Bain NT, Madan P, Betts DH. The early embryo response to intracellular reactive oxygen species is developmentally regulated. Reprod Fertil Dev 2011; 23:561-575. [ Links ]

Behl R, Pandey RS. FSH induced stimulation of catalase activity in goat granulosa cells in vitro. Anim Reprod Sci 2002; 70:215-221. [ Links ]

Ben-Meir A, Burstein E, Borrego-Alvarez A, Chong J, Wong E, Yavorska T, Naranian T, Chi M, Wang Y, Bentov Y, Alexis J, Meriano J, Sung HK, Gasser DL, Moley KH, Hekimi S, Casper RF, Jurisicova A. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell 2015; 14:887-895. [ Links ]

Benedetti S, Tagliamonte MC, Catalani S, Primiterra M, Canestrari F, De Stefani S, Palini S, Bulletti C. Differences in blood and semen oxidative status in fertile and infertile men, and their relationship with sperm quality. Reprod Biomed Online 2012; 25:300-306. [ Links ]

Bernabucci U, Ronchi B, Lacetera N, Nardone A. Influence of body conditions score on relationships between metabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci 2005; 88:2017-2026. [ Links ]

Bourne N, Wathes DC, McGowan M, Laven R. A comparison of the effects of parenteral and oral administration of supplementary vitamin E on plasma vitamin E concentrations in dairy cows at different stages of lactation. Livestock Sci 2007; 10:57-64. [ Links ]

Brännström M, Enskog A. Leukocyte networks and ovulation. J Reprod Immunol 2002; 57:47-60. http://www.jrijournal.org/article/S0165-0378(02)00009-8/abstract. [ Links ]

Braw-Tal R, Yossefi S. Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J Reprod Fertil 1997; 109:165-171. [ Links ]

Britt JH. Oocyte development in cattle: physiological and genetic aspects. R Bras Zootec 2008; 37:110-115. [ Links ]

Buttler WR. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livest Prod Sci 2003; 83:211-218. [ Links ]

Celi P, Gabai G. Oxidant/antioxidant balance in animal nutrition and health: the role of protein oxidation. Front Vet Sci 2015; 2:1-13. [ Links ]

Celi P, Merlo M, Da Dalt L, Stefani A, Barbato O, Gabai G. Relationship between late embryonic mortality and the increase in plasma advanced oxidized protein products (AOPP) in dairy cows. Reprod Fertil Dev 2011; 23:527-533. [ Links ]

Chaube SK, Prasad PV, Thakur SC, Shrivastav TG. Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro. Apoptosis 2005; 10:863-874. [ Links ]

Cigliano L, Strazzullo M, Rossetti C, Grazioli G, Auriemma G, Sarubbi F, Iannuzzi C, Iannuzzi L, Spagnuolo MS. Characterization of blood redox status of early and mid-late lactating dairy cows. Czech J Anim Sci 2014; 59:170-181. [ Links ]

Cingi CC, Baser DF, Karafakioglu YS, Fidan AF. Stress response in dairy cows related to rectal examination. Acta Sci Vet 2012; 40:1053. [ Links ]

Combelles CM, Holick EA, Paolella LJ, Walker DC, Wu Q. Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reprod 2010; 139:871-881. [ Links ]

De Bie J, Langbeen A, Verlaet AAJ, Florizoone F, Immig I, Hermans N, Fransen E, Bols PEJ, Leroy JLMR. The effect of a negative energy balance status on β-carotene availability in serum and follicular fluid of nonlactating dairy cows. J Dairy Sci 2016; 99:5808-5819. [ Links ]

De Rensis F, Lopez-Gatius F, García-Ispierto I, Morini G, Scaramuzzi RJ. Causes of declining fertility in dairy cows during the warm season. Theriogenology 2017; 91:145-153. [ Links ]

Dias FC, Khan MI, Sirard MA, Adams GP, Singh J. Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reprod 2013; 146:181-191. [ Links ]

Ealy AD, Drost M, Hansen PJ. Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J Dairy Sci 1993; 76:2899-2905. [ Links ]

Eberhardt DM, Will WA, Godkin JD. Retinol administration to superovulated ewes improves in vitro embryonic viability. Biol Reprod 1999; 60:1483-1487. [ Links ]

Fortune JE, G. Rivera MAC, Turzillo AM. Differentiation of dominant versus subordinate follicles in cattle. Biol Reprod 2001; 65:648-654. [ Links ]

Ginther OJ. Selection of the dominant follicle in cattle and horses. Anim Reprod Sci 2000; 60-61:61-79. [ Links ]

Gonzalez-Maldonado J, Rangel-Santos R, Rodriguez-De Lara R, Ramirez-Valverde G. Impacts of vitamin C and E injections on ovarian structures and fertility in Holstein cows under heat stress conditions. Turk J Vet Anim Sci 2017; 41:345-350 [ Links ]

Guérin P, El Mouatassim S, Ménézo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 2001; 7:175-189. [ Links ]

Gupta S, Banerjee J, Agarwal A. The impact of reactive oxygen species on early human embryos: a systematic review of the literature. Embryo Talk 2006; 1.2:87-98. [ Links ]

Gupta S, Choi A, Yu HY, Czerniak SM, Holick EA, Paolella LJ, Agarwal A, Combelles CM. Fluctuations in total antioxidant capacity, catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis. Reprod Fertil Dev 2011; 23:673-680. [ Links ]

Halliwell B, Gutteridge JM. The definition and measurement of antioxidants in biological systems. Free Radic Biol Med 1995; 18:125-126. [ Links ]

Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. Br J Pharmacol 2004; 142:231-255. [ Links ]

Hansen PJ. Cellular and molecular basis of therapies to ameliorate effects of heat stress on embryonic development in cattle. Anim Reprod 2013; 10:322-333. [ Links ]

Hanukoglu I, Rapoport R, Weiner L, Sklan D. Electron leakage from the mitochondrial NADPH-adrenodoxin reductase- adrenodoxin-P450scc (cholesterol side chain cleavage) system. Arch Biochem Biophys 1993; 305:489-498. [ Links ]

Hayashi K, Miyamoto A, Konari A, Ohtani M, Fukui Y. Effect of local interaction of reactive oxygen species with prostaglandin F (2 alpha) on the release of progesterone in ovine corpora lutea in vivo. Theriogenology 2003; 59:1335-1344. [ Links ]

Hennet ML, Yu HY, Combelles CM. Follicular fluid hydrogen peroxide and lipid hydroperoxide in bovine antral follicles of various size, atresia, and dominance status. J Assist Reprod Genet 2013; 30:333-340. [ Links ]

Hozyen FH, H Ahmed H, Essawy GE, Shalaby SI. Seasonal changes in some oxidant and antioxidant parameters during folliculogenesis in Egyptian buffalo. Anim Reprod Sci 2014; 151:131-136. [ Links ]

Jan MH, Das GK, Khan FA, Singh J, Bashir ST, Khan S, Prasad JK, Mehrotra S, Pathak MC, Singh G, Sarkar M. Evaluation of follicular oxidant-antioxidant balance and oxidative damage during reproductive acyclicity in water buffalo (Bubalus bubalis). Asian Pacif J Reprod 2014; 3:35-40. [ Links ]

Kahlon RS, Singh R. Effect of α-tocopherol supplementation on plasma levels of antioxidant vitamins in anestrus buffalo heifers (Bubalus bubalis). Asian-Aust J Anim Sci 2004; 17:1088-1092. [ Links ]

Kala M, Vaseem Shaikh M, Nivsarkar M. Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol 2016. 16:28-35. [ Links ]

Kato H, Sugino N, Takiguchi S, Kashida S, Nakamura Y. Roles of reactive oxygen species in the regulation of luteal function. Reproduction 1997; 2:81-83. [ Links ]

Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can J Physiol Pharmacol 2010; 88:399-413. [ Links ]

Komatsu K, Iwase A, Mawatari M, Wang J, Yamashita M, Kikkawa F. Mitochondrial membrane potential in 2-cell stage embryos correlates with the success of preimplantation development. Reprod 2014; 147:627-638. [ Links ]

Kizil O, Akar Y, Saat N, Kizil M, Yuksel M. The plasma lipid peroxidation intensity (MDA) and chain-breaking antioxidant concentrations in the cows with clinic or subclinic mastitis. Revue Méd Vét 2007; 158:529-533. [ Links ]

Jancar N, Kopitar AN, Ihan A, Virant Klun I, Bokal EV. Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilization and blastocyst development. J Assist Reprod Genet 2007; 24:91-97. [ Links ]

Lavon Y, Ezra E, Leitner G, Wolfenson D. Association of conception rate with pattern and level of somatic cell count elevation relative to time of insemination in dairy cows. J Dairy Sci 2011; 94:4538-4545. [ Links ]

Leroy JL, Vanholder T, Delanghe JR, Opsomer G, Van Soom A, Bols PE, Dewulf J, de Kruif A. Metabolic changes in follicular fluid of the dominant follicle in high-yielding dairy cows early post partum. Theriogenology 2004; 62:1131-1143. [ Links ]

Leroy JL,Vanholder T, Opsomer G,Van Soom A, de Kruif A.Theinvitro development of bovine oocytes after maturation in glucose and beta-hydroxybutyrate concentrations associated with negative energy balance in dairy cows. Reprod Domest Anim 2006; 41:119-123. [ Links ]

Leroy JL, Vanholder T, Mateusen B, Christophe A, Opsomer G, de Kruif A, Genicot G, Van Soom A. Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction 2005; 130:485-495. [ Links ]

Leung FY. Trace elements that act as antioxidants in parenteral micronutrition. J Nutr Biochem 1998; 9:304-307. http://www. jnutbio.com/article/S0955-2863(98)00018-7/abstractLinks ]

Liu Y, He XQ, Huang X, Ding L, Xu L, Shen YT, Zhang F, Zhu MB, Xu BH, Qi ZQ, Wang HL. Resveratrol protects mouse oocytes from methylglyoxal-induced oxidative damage. Plos One 2013; 8:1-8. [ Links ]

Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn Rev 2010; 4:118-126. [ Links ]

Louis GM, Cooney MA, Lynch CD, Handal A. Periconception window: advising the pregnancy-planning couple. Fertil Steril 2008; 89:119-121. [ Links ]

Luck MR, Zhao Y. Identification and measurement of collagen in the bovine corpus luteum and its relationship with ascorbic acid and tissue development. J Reprod Fertil 1993; 99:647-652. [ Links ]

Lucy MC, McDougall S, Nation DP. The use of hormonal treatments to improve the reproductive performance of lactating dairy cows in feedlot or pasture-based management systems. Anim Reprod Sci 2004; 82-83:495-512. [ Links ]

Magata F, Horiuchi M, Echizenya R, Miura R, Chiba S, Matsui M, Miyamoto A, Kobayashi Y, Shimizu T. Lipopolysaccharide in ovarian follicular fluid influences the steroid production in large follicles of dairy cows. Anim Reprod Sci 2014; 144:6-13. [ Links ]

Manes J, Campero C, Hozbor F, Alberio R, Ungerfeld R. Vaginal histological changes after using intravaginal sponges for oestrous synchronization in anoestrous ewes. Reprod Domest Anim 2015; 50:270-274. [ Links ]

Manes J, Fiorentino MA, Kaiser G, Hozbor F, Alberioa R, Sanchez E, Paolicchi F. Changes in the aerobic vaginal flora after treatment with different intravaginal devices in ewes. Small Rumin Res 2010; 94:201-204. [ Links ]

Manes J, Hozbor F, Alberioa R, Ungerfeld R. Intravaginal placebo sponges affect negatively the conception rate in sheep. Small Rumin Res 2014; 120:108-111. [ Links ]

McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21:200-214. [ Links ]

Menchaca AZ, Neto CDS, Cuadro F. Estrous synchronization treatments in sheep: brief update. Rev Bras Reprod Anim 2017; 41:340-344. [ Links ]

Mokhber-Dezfouli MR, Rahimikia E, Asadi F, Nadalian MG. The role of route of vitamin E administration on the plasma antioxidant activity and lipid peroxidation in newborn calves. Basic Clin Pharmacol Toxicol 2008; 103:414-418. [ Links ]

Morales H, Tilquin P, Rees JF, Massip A, Dessy F, Van Langendonckt A. Pyruvate prevents peroxide-induced injury of in vitro preimplantation bovine embryos. Mol Reprod Dev 1999; 52:149-157. [ Links ]

Nabenishi H, Takagi S, Kamata H, Nishimoto T, Morita T, Ashizawa K, Tsuzuki Y. The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Mol Reprod Dev 2012; 79:31-40. [ Links ]

Nakao T, Sato T, Moriyoshi M, Kawata K. Plasma cortisol response in dairy cows to vaginoscopy, genital palpation per rectum and artificial insemination. Zentralbl Veterinarmed A 1994; 41:16-21. [ Links ]

Nayyar S, Jindal R. Essentiality of antioxidant vitamins for ruminants in relation to stress and reproduction. Iranian J Vet Res 2010; 11:1-9. [ Links ]

Ozawa M, Hirabayashi M, Kanai Y. Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reprod 2002; 124:683-689. [ Links ]

Pandey AN, Chaube SK. A moderate increase of hydrogen peroxide level is beneficial for spontaneous resumption of meiosis from diplotene arrest in rat oocytes cultured in vitro. Biores Open Access 2014; 3:183-191. [ Links ]

Park SJ, Kim TS, Kim JM, Chang KT, Lee HS, Lee DS. Repeated superovulation via PMSG/hCG administration induces 2-cys peroxiredoxins expression and overoxidation in the reproductive tracts of female mice. Mol Cells 2015; 38:1071-1078. [ Links ]

Pedernera M, Celi P, García SC, Salvin HE, Barchia I, Fulkerson WJ. Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Vet J 2010; 186:352-357. [ Links ]

Pérez-Crespo M, Ramírez MA, Fernández-González R, Rizos D, Lonergan P, Pintado B, Gutiérrez-Adán A. Differential sensitivity of male and female mouse embryos to oxidative induced heat-stress is mediated by glucose-6- phosphate dehydrogenase gene expression. Mol Reprod Dev 2005; 72:502-510. [ Links ]

Phaniendra A, Jestadi DB, Periyasamy L. Free radicals: properties, sources, targets, and their implication in various diseases. Indian J Clin Biochem 2015; 30:11-26. [ Links ]

Pisoschi AM, Pop A. The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 2015; 97:55-74. [ Links ]

Poston L, Igosheva N, Mistry HD, Seed PT, Shennan AH, Rana S, Karumanchi SA, Chappell LC. Role of oxidative stress and antioxidant supplementation in pregnancy disorders. Am J Clin Nutr 2011; 94:1980S-1985S. [ Links ]

Prasad S, Tiwari M, Pandey AN, Shrivastav TG, Chaube SK. Impact of stress on oocyte quality and reproductive outcome. J Biomed Sci 2016; 23:1-5. [ Links ]

Quirk SM, Cowan RG, Harman RM, Hu CL, Porter DA. Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J Anim Sci 2004; 82:E40-E52. [ Links ]

Rahman ANMA, Abdullah RB, Wan-Khadijah WE. Estrus synchronization and superovulation in goats: a review. J Biol Sci 2008; 8:1129-1137. [ Links ]

Ratchford AM, Esguerra CR, Moley KH. Decreased oocyte- granulosa cell gap junction communication and connexin expression in a type 1 diabetic mouse model. Mol Endocrinol 2008; 22:2643-2654. [ Links ]

Rizzo A, Minoia G, Trisolini C, Manca R, Sciorsci RL. Concentrations of free radicals and beta-endorphins in repeat breeder cows. Anim Reprod Sci 2007; 100:257-263. [ Links ]

Rizzo A, Minoia G, Trisolini C, Mutinati M, Spedicato M, Jirillo F, Sciorsci RL. Reactive oxygen species (ROS): involvement in bovine follicular cysts etiopathogenesis. Immunopharmacol Immunotoxicol 2009; 31:631-635. [ Links ]

Rizzo A, Roscino MT, Binetti F, Sciorsci RL. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim 2012; 47:344-352. [ Links ]

Roth Z. Physiology and endocrinology symposium: cellular and molecular mechanisms of heat stress related to bovine ovarian function. J Anim Sci 2015; 93:2034-2044. [ Links ]

Roth Z, Asaf S, Furman O, Lavon Y, Kalo D, Wolfenson D, Leitner G. Subclinical mastitis disrupts oocyte cytoplasmic maturation in association with reduced developmental competence and impaired gene expression in preimplantation bovine embryos. Reprod Fertil Dev 2015; 28(11) 1653-1662. [ Links ]

Sales JNS, Pereira RVV, Bicalho RC, Baruselli PS. Effect of injectable copper, selenium, zinc and manganese on the pregnancy rate of crossbred heifers (Bos indicus×Bos taurus) synchronized for timed embryo transfer. Livestock Sci 2011; 142:59-62. [ Links ]

Sales JN, Dias LM, Viveiros AT, Pereira MN, Souza JC. Embryo production and quality of Holstein heifers and cows supplemented with beta-carotene and tocopherol. Anim Reprod Sci 2008; 106:77-89. [ Links ]

Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank MC. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J Dairy Sci 2002; 85:2803-2812. [ Links ]

Schweigert FJ, Zucker H. Concentrations of vitamin A, beta- carotene and vitamin E in individual bovine follicles of different quality. J Reprod Fertil 1988; 82:575-579. [ Links ]

Shahid M, Gao J, Zhou Y, Liu G, Ali T, Deng Y, Sabir N, Su J, Han B. Prototheca zopfii isolated from bovine mastitis induced oxidative stress and apoptosis in bovine mammary epithelial cells. Oncotarget 2017; 8:31938-31947. [ Links ]

Sharma L, Kumar AK, Rahal A, Kumar A, Nigam R. Relationship between serum biomarkers and oxidative stress in dairy cattle and buffaloes with clinical and sub-clinical mastitis. Biotechnol 2016; 15:96-100. [ Links ]

Shen M, Lin F, Zhang J, Tang Y, Chen WK, Liu H. Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress. J Biol Chem 2012; 287:25727-25740. [ Links ]

Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N. Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci USA 2011; 108:1462-1467. [ Links ]

Silva JP, Coutinho OP. Free radicals in the regulation of damage and cell death - basic mechanisms and prevention. Drug Discov Ther 2010; 4:144-167. [ Links ]

Song Y, Li N, Gu J, Fu S, Peng Z, Zhao C, Zhang Y, Li X, Wang Z, Li X, Liu G. β-hydroxybutyrate induces bovine hepatocyte apoptosis via an ROS-p38 signaling pathway. J Dairy Sci 2016; 99:9184-9198. [ Links ]

Song Y, Li X, Li Y, Li N, Shi X, Ding H, Zhang Y, Li X, Liu G, Wang Z. Non-esterified fatty acids activate the ROS-p38-p53/ Nrf2 signaling pathway to induce bovine hepatocyte apoptosis in vitro. Apoptosis 2014; 19:984-997. [ Links ]

Sönmez M, Bozkurt T, Türk G, Gür S, Kizil M, Yüce A. The effect of vitamin E treatment during preovulatory period on reproductive performance of goats following estrous synchronization using intravaginal sponges. Anim Reprod Sci 2009; 114:183-192. [ Links ]

Suárez G, Zunino P, Carol H, Ungerfeld R. Changes in the aerobic vaginal bacterial mucous load and assessment of the susceptibility to antibiotics after treatment with intravaginal sponges in anestrous ewes. Small Rumin Res 2006; 63:39-43. [ Links ]

Takahashi M. Heat stress on reproductive function and fertility in mammals. Reprod Med Biol 2012; 11:37-47. [ Links ]

Talukder S, Ingenhoff L, Kerrisk KL, Celi P. Plasma oxidative stress biomarkers and progesterone profiles in a dairy cow diagnosed with an ovarian follicular cyst. Vet Q 2014a; 34:113- 117. [ Links ]

Talukder S, Kerrisk KL, Gabai G, Fukutomi A, Celi P. Changes in milk oxidative stress biomarkers in lactating dairy cows with ovulatory and an-ovulatory oestrous cycles. Anim Reprod Sci 2015; 158:86-95. [ Links ]

Talukder S, Kerrisk KL, Ingenhoff L, Gabai G, Garcia SC, Celi P. Changes in plasma oxidative stress biomarkers in dairy cows after oestrus synchronisation with controlled internal drug release (CIDR) and prostaglandin F2α (PGF2α). Anim Prod Sci 2014b; 54:1490-1496. [ Links ]

Tripathi A, Kumar KV, Chaube SK. Meiotic cell cycle arrest in mammalian oocytes. J Cell Physiol 2010; 223:592-600. [ Links ]

Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG, Chaube SK. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radic Res 2009; 43:287-294. [ Links ]

Van Hoeck V, Leroy JL, Arias Alvarez M, Rizos D, Gutierrez- Adan A, Schnorbusch K, Bols PE, Leese HJ, Sturmey RG. Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 2013; 145:33-44. [ Links ]

Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39:44-84. [ Links ]

Vierk JE, Murdoch WJ, Austin KJ, Van Kirk EA, Hansen TR. Antiluteolytic effect of alpha tocopherol in ewes. J Anim Sci 1998; 81:372. [ Links ]

Vu HV, Dam TV, Acosta TJ. Regulation of superoxide dismutase by prostaglandin F2α in the bovine corpus luteum. Anim Reprod 2013; 10:88-98. [ Links ]

Vu HV, Lee S, Acosta TJ, Yoshioka S, Abe H, Okuda K. Roles of prostaglandin F2alpha and hydrogen peroxide in the regulation of Copper/Zinc superoxide dismutase in bovine corpus luteum and luteal endothelial cells. Reprod Biol Endocrinol 2012; 10:87. [ Links ]

Walsh RB, LeBlanc SJ, Duffield TD, Kelton DF, Walton JS, Leslie KE. Synchronization of estrus and pregnancy risk in anestrous dairy cows after treatment with a progesterone-releasing intravaginal device. J Dairy Sci 2007; 90:1139-1148. [ Links ]

Wolfenson D, Leitner G, Lavon Y. The disruptive effects of mastitis on reproduction and fertility in dairy cows. Ital J Anim Sci 2015; 14:650-654. [ Links ]

Yacobi K, Tsafriri A, Gross A. Luteinizing hormone-induced caspase activation in rat preovulatory follicles is coupled to mitochondrial steroidogenesis. Endocrinology 2007; 148:1717-1726. [ Links ]

Yildiz A, Balikçi E, Gürdoğan F. Effect of injection of vitamin e and selenium administered immediately before the ovsynch synchronization on conception rate, antioxidant activity and progesterone levels in dairy cows. FÜ Sağ Bil Vet Derg 2015; 29:183-186. [ Links ]

Zhao SJ, Pang YW, Zhao XM, Du WH, Hao HS, Zhu HB. Effects of lipopolysaccharide on maturation of bovine oocyte in vitro and its possible mechanisms. Oncotarget 2017; 8:4656-4667. [ Links ]

¤ To cite this article: Gonzalez-Maldonado J, Martínez-Aispuro JA, Rangel-Santos R, Rodríguez-de Lara R. Antioxidant supplementation in female ruminants during the periconceptional period: A review. Rev Colomb Cienc Pecu 2018; 31(4):245-255.

Received: September 29, 2016; Accepted: February 14, 2018

* Corresponding author: Juan Gonzalez-Maldonado. Posgrado en Producción Animal, Departamento de Zootecnia, Universidad Autónoma Chapingo, km 38.5 carretera México-Texcoco, Chapingo, Estado de México, C.P. 56230. E-mail: gomajuan22@hotmail.com.

Conflicts of interest

The authors declare they have no conflicts of interest with regard to the work presented in this report.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License