Can thermoregulatory response to heat stress be improved in lactating dairy cows? Insights from counter-current heat transfer systems impacting reproduction

Abstract

Climate change has caused heat stress (HS) to become an increasingly severe problem for high-producing dairy herds. Although cooling systems allow milk production to remain nearly constant throughout the year, fertility decreases during summer. Physiological counter-current heat transfer mechanisms maintaining brain/hypothalamic and reproductive functions in cattle are vulnerable to HS. In this study, I propose strategies to improve cooling systems, particularly in zones with the highest risk of increased body temperature, such as milking areas. In addition, heat transfer mechanisms to protect the brain–hypothalamus axis from hyperthermia must be considered when implementing measures to reduce HS-related problems.

Introduction

Global warming is a recurring and growing environmental concern. Hyperthermia, defined as an increase in body temperature above the homeothermic point (heat stress [HS]), compromises the physiological functions of mammals. Over the last two decades, particularly in the past few years, there has been tremendous interest in thermoregulatory response to thermal stress in animals and humans [1, 2]. Although there is a greater or lesser response to HS between different species, breeds, and individuals, dairy cattle are particularly susceptible to metabolic stress related to milk production. The heat-induced impairment of reproductive functions [3, 4] attests to the global scale of HS-related problems in the dairy industry, where production and reproduction are strictly monitored. Cooling strategies, such as the short-term spraying of water followed by its evaporation from the skin using air from fans to alleviate the effects of the summer thermal environment [5, 6], can help maintain milk production throughout the year [3]. However, fertility remains much lower during the warm period than during the cold period of the year. For example, data from extensive studies show that conception during the warm period is 62–81% of that during the cold period [3, 7, 8]. Therefore, cooling systems leave much scope for improvement in terms of reproductive functions. In this study, I focus on the physiological mechanisms underlying counter-current heat transfer, particularly regarding their effects on reproductive functions in dairy cows. Herein, I propose monitoring and improving cooling systems in feeding and milking areas and the area exposed to maximum HS, i.e., the waiting room of the milking parlor. Brain cooling through counter-current mechanisms can help mitigate the adverse effects of HS in lactating dairy cows. Heat transfer through such mechanisms is primarily passive and does not need a transport system. The mechanisms described herein mainly involve heat transfer from a vein to an artery.

Heat transfer in the head

The brain is the first organ damaged by high temperatures [9]. The cooling of the brain through respiratory air flow via nasal passage has been extensively described in artiodactyls, including cattle [10, 11]. A vascular counter-current heat exchanger called carotid rete, located within the cavernous sinus at the base of the brain (Fig. 1), is implicated in brain cooling. Nasal venous flow, cooled by evaporation in the nasal cavity, in turn, cools carotid blood through local heat transfer in the carotid artery–cavernous sinus complex. This system, regarded as a physiological feature for surviving climate change [12], provides rapid heat exchange to reduce brain temperature below body temperature [13]. Among the consequences of brain cooling is a reduction in hypothalamic temperature, with the hypothalamus being the principal brain region for regulating thermal homeostasis [12, 14]. Brain cooling failure is associated with inappropriate hypothalamic and hypophyseal hormone secretions [9]. Thus, environmental thermal stress can either directly affect the ovary or indirectly affect it by affecting the brain–hypothalamus axis or both simultaneously, which is likely to be the case under severe HS. In all cases, the physiology of the hypothalamic–pituitary–gonadal axis is impaired. Therefore, brain cooling through counter-current mechanisms must be used to reduce the effects of HS on reproduction. Examples include a stream of cold air on the face and in the nostrils of cows [4]. Although primates do not have a carotid rete [12], intranasal brain cooling is a promising clinical intervention for acute ischemic stroke in humans [15].

Fig. 1.

Drawing depicting the position of the carotid rete in cattle. During the cooling of the brain–hypothalamus axis, cold venous blood from the nasal mucosa drains into the cavernous sinus via the angularis oculi vein. Drawing adapted from Strauss et al. [12] and Baker [13].

Heat transfer in the reproductive system

Changes in the secretion of steroid hormones from the ovary during sexual cycle phases impact the establishment of temperature gradients within the ovary, its closest neighbor, i.e., the oviduct, and throughout the genital tract. The local cooling of the female reproductive system, particularly of specific ovarian and oviductal tissues, occurs close to ovulation, favoring male and female gamete maturation [4, 16, 17]. Pre-ovulatory follicles may be over 1.0 ºC cooler than ovarian stroma, and both compartments may be cooler than their neighboring tissues [18, 19]. The low temperature of follicular fluid permits mammalian ovulation [20, 21], and such cooling correlates positively with the potential for pregnancy in dairy cows [22,23,24]. During the pre-ovulatory period, sperm pass from the warmer uterus through the uterotubal junction into a cooler isthmus, wherein they exhibit reduced motility and are stored until ovulation [16, 25]. However, the final process of follicle cooling before ovulation is highly sensitive to HS [4].

In addition, the counter-current transfer of heat from venous blood, interstitial fluid, and lymph to the arterial blood of maturing follicles, as well as heat transfer between vessels in ovarian hilus, may favor the maintenance of such temperature gradients in both ovarian and oviductal tissues [9, 26]. The oocyte-mediated regulation of ovarian follicular development is a possible factor that induces cooling processes in the reproductive system. Communication between oocytes and surrounding somatic cells is bidirectional [27,28,29]. In addition, the oocyte may prompt processes leading to the ovulation of a responsive Graafian follicle [30]. As oocytes have existed in evolutionary history in the form of isolated groups of germ cells before the development of specific follicular cells, the cooling of pre-ovulatory follicles may be traced back to the primitive stages of external fertilization, wherein the aggregates of oocytes are shed into freshwater. The oocyte is particularly sensitive to HS [3]; therefore, a damaged oocyte could show a reduced competence to favor follicular cooling and ovulation. Furthermore, a period of 2–3 estrous cycles appears to be required after heat damage until recovery of competent oocytes [31]. In this case, ovulation failure may occasionally result from prior oocyte damage because of HS. If this interpretation is correct, cooling systems must be used for periods longer than the duration of estrus, thus covers the entire period of exposure to HS conditions.

Strategies at herd level

As noted above, although cooling systems help maintain high milk production at similar levels during the warm and cold periods, reproductive parameters are reduced under HS. In herds under our surveillance, if the conception rate is more than 80% lower at the beginning of the warm period than in the cold period, body temperature is measured throughout the day in a group of cows. Stress events may be identified using a data logger thermosensor attached to an intravaginal drug release device, which enables the detection of thermal stress situations in the daily routine of a cow [32,33,34]. Over the last few years, time spent in the waiting room before milking has been among the causes of maximum exposure to thermal stress, in agreement with the results of previous studies on dairy herds under grazing conditions [35,36,37]. An increase of up to 2°C in body temperature is recorded, even during winter. Consequently, for evaluating the application of the cooling systems, the fans are programmed to be activated when the temperature in the waiting area reaches 10ºC, and the water sprinklers are activated at 18ºC and above until the temperature in the waiting area is restored to the optimal range. Therefore, cooling systems are now activated year-round in milking areas, with trial and error by farm managers leading to positive results for reproduction. These results have been derived from the farms in our geographical area; thus, the effectiveness of cooling systems in the milking areas of intensive farms has not been explored in general. Therefore, it is necessary to conduct studies to elucidate the efficacy of using cooling systems in the milking areas of intensive farms and provide guidelines for using cooling systems before and during milking. The increased use of ventilation and water sprinkler systems may facilitate using heat exchanger systems for brain cooling. In the groups of cows waiting for milking, we observed that most held their heads up, favoring nasal cooling and thus of the carotid artery–cavernous sinus complex. The impact of HS on lactating dairy cows is greatly reduced when inspired air is cooled 19–28ºC below ambient air temperature [38]. Moreover, cooling systems in the eating and resting areas must be continuously monitored.

Concluding remarks

In dairy herds under ever-increasing pressures to improve reproductive efficiency, efforts to apply effective cooling systems must focus on eating and resting areas and farm sites where cows exhibit increased body temperature. Counter-current heat transfer in both the reproductive tract and head is a physiological trait supporting reproductive function and is highly sensitive to HS. The cooling of the brain–hypothalamus axis through counter-current mechanisms must be considered when implementing measures to reduce HS-related problems.

Conflict of interests

The authors declare no conflicts of interest.