The Impact of Heat Stress on the Physiological, Productive, and Reproductive Status of Dairy Cows

Abstract

Climate change is a global problem with an important influence on farm animals, so the entire veterinary medical industry is working to combat the effects of heat stress. In recent years, global warming has been correlated with physiological changes in adaptation that lead to a decrease in milk production and quality. We have chosen to study these mechanisms that are based on hormonal imbalances (LH, TSH, and prolactin) and general imbalances (apathy and lack of appetite).

1. Introduction

Climate change is a real problem with a significant impact on the entire globe, having the ability to influence the quality of life of all animal species. For Romania, climate change, especially in the southern part, is dominated by a large-scale aridization determined by the increase in maximum temperatures, the prolongation of warm periods, and the decrease in the annual level of precipitation recorded [1].

At the same time, cow farming is one of the most important sources of global food. Studies and reports have shown that approximately 33% of the proteins consumed globally come from livestock productions, and for Romania, approximately 14.97% of the energy and proteins consumed are based on these livestock productions [2].

Based on these data, we can argue that the problems correlated with climate change constitute a real issue for the livestock industry and food security. The maximum temperature values, associated with the extension of warm periods and the decrease in rainfall levels, lead to a decrease in the availability and quality of feed, respectively. The reduction in nutritional principles is necessary for the maintenance of tools involved in supporting reproduction, production, and general health [3].

An indirect effect of climate change, but with a significant impact on the welfare of farm animals, is the multiplication of vectors and/or pathogens, as well as the expansion of their ability to survive for longer periods of time. This directly results in an increase in the rate of specific diseases and a faster expansion in livestock [4].

Of all the species of animals of economic interest, it seems that the dairy cow breeding industry is the most severely affected by climate change due to the metabolic effort sustained to sustain milk production at a high level; in this way, heat stress can cause important economic losses. This is very crucial for the adaptive efforts that animals try to develop because more energy will be used to support vital activities and less for the production pathways. However, the adverse effects of heat stress on productive and reproductive indices depend on the species, breeds, and especially the management practices specific to each region.

This review includes documentation regarding the impact of heat stress on livestock. Efforts were made to describe the main adaptation mechanisms to heat stress challenges and the impact on the productive and reproductive capabilities of these animals during hot periods. Also, some advanced systems available for monitoring heat stress responses were covered. In addition, several ameliorative strategies are revised, which may help animals better adapt to heat stress.

2. Relevant Sections

Generally, heat stress is represented by the non-specific physiological response of animals to external thermal values when they produce more heat than they can dissipate [5]. Body temperature is an important physiological indicator for the health of animals, including dairy cows. When the ambient temperature exceeds normal body temperature, dairy cows must activate their physiological heat dissipation mechanisms. Numerous studies have shown that during warm seasons animals endure transient increases in body temperature, increased heart rate, and increased respiratory rate [6], associated with a significant decrease in intake [7], milk production [8], and reproductive performance [9].

These physiological adaptation mechanisms allow animals to efficiently dissipate accumulated heat through evaporation.

However, the capacity of dairy cows to dissipate heat by evaporation from the surface of the skin is somewhat limited due to the reduced body surface area relative to the weight of the animals, poorly developed sweat glands, and hairiness on the surface of the body [5].

Moreover, a significant amount of heat results from rumen fermentation processes [10]. As a result, dairy cows are much more prone to the unfavorable action of high temperatures during warm seasons.

3. Discussion

3.1. Body Temperature

The well-being and checking of heat stress in dairy cattle has become a priority for veterinarians, the negative effect being amplified by the large number of affected subjects, decrease in milk production, and increase in metabolic needs; thus, within the farm, the thermal balance is ensured by equalizing the heat generated by the animal during daily activities with the heat lost in the environment. Under common conditions, the oscillations in body temperature are very small. Cattle temperature normally fluctuates between 38 and 39 °C with a diurnal variation of ±0.5 °C depending on environmental temperature, peaking in the early evening and reaching a minimum in the early morning. Fulminant episodes of heat stress can require long periods of several weeks to adapt to fluctuating temperatures [11]. Multiparous cows are prone to more heat stress than primiparous cows. Acatincai et al. [12] detected that with an increase in air temperature above 27 to 28 °C, the rumination process was severely affected in Romanian Black and White multiparous cows.

The climate of Romania is continental, transitioning into humid subtropical; thus, four seasons with variable temperatures are delimited during the 12 months. Several studies indicate that in these environmental conditions, heat stress can persist for several months [11]. Other studies claim that the optimal body temperature in thermo-neutral conditions is between 38 and 39.2 °C, and the recommended ambient temperature is between 16 °C and 25 °C. In areas with subtropical climates at night there are no significant drops in temperature, ruminants being diurnal animals that produce a greater amount of heat during the day compared to the night period, and when the temperature and humidity of the environment do not drop sufficiently during the night, continuous heat stress occurs. In these conditions, body temperature rises and may lead to prolonged elevations above tolerance levels that may cause damage to body tissues and organs and even morbidity (Figure 1).

Traditionally, rectal temperature has been regarded as a reliable indicator of a cow’s body temperature, but continuous measurement is very limited. Furthermore, most body temperature monitoring methods are not performed in real-time and are primarily used for research purposes, with limited availability for commercial farms.

Nowadays, various methods exist to measure how farm animals respond to heat stress, which can be classified as either invasive or non-invasive from an animal welfare perspective.

Infrared thermography (IRT) represents a cutting-edge, non-invasive technique for assessing stress responses, productivity, health, and overall welfare in farm animals. Various remote sensing technologies, including ear canal sensors, rumen boluses, rectal and vaginal probes, IRT, and implantable microchips, can be employed in grazing animals to evaluate the degree of heat stress they endure [13]. As 60% of heat is dissipated within the infrared range, this approach could serve as a marker for stress reactions. An infrared camera picks up the body’s heat emissions using infrared sensors and showcases them as a thermogram with pixels of different colors or shades, indicating various infrared temperatures of the animal. Relevant software should be used to analyze the minimum, maximum, and average IRT of user-targeted body surface areas from every thermal image. In the majority of research, a clear pattern was seen in eye temperature changes in response to stress, starting with a decrease and then rising above the initial level [14]. Infrared thermography (IRT) imaging and videos necessitate a controlled environment, which involves additional cattle handling for data acquisition and sophisticated software for analysis. For instance, IRT-based measurements of forehead and body surface temperature can vary even under similar temperature–humidity index (THI) conditions. Moreover, raw IRT video data exhibit poor correlation with internal body temperature and thermal status in cattle, requiring extensive data manipulation for effective use.

Automated, sensor-based, real-time measurement systems offer a promising alternative by enabling close monitoring of body temperature. These systems facilitate the early prediction of heat stress and diseases while upholding the highest standards of animal welfare and minimizing human intervention. Technologies such as temperature-sensing ear tags, rumen-reticular boluses, intra-rectal and intra-vaginal devices, and wearable and implantable microchips with remote data transmission capabilities require further development to enhance heat stress prediction models based on real-time temperature data. Additionally, ingestible biosensors and radiofrequency identification (RFID) sensors can monitor the internal temperature of cattle, providing data linked to individual animal identities.

Sweating and panting were considered two of the physiological responses in animals subjected to heat stress; another parameter identified in these situations is the increase in heart rate to the stimulation of the sinoatrial node [15]. A respiration rate of less than 40 breaths per minute is generally considered normal for dairy cattle, although a slightly higher value of around 60 breaths per minute is also deemed acceptable. Under severe heat stress conditions, the respiration rate can exceed 150 breaths per minute. In some cases, severe stress may cause a shift between “rapid–shallow” and “slow–deep” breathing, leading to a reduction in respiration rate. Visual assessment of respiration rate is time-consuming and challenging to maintain accurately from the considerable distance needed to minimize animal disturbance. Additionally, respiration rate alone does not account for respiratory dynamics such as drooling and open-mouth panting, which are associated with increasing heat stress.

Since heart rate and respiration rate are positively correlated, heart rate can serve as a potential indicator of heat stress, considering individual variations in panting ability. This makes heart rate useful for assessing short-term heat response, while additional parameters like respiration rate and body temperature are necessary for monitoring prolonged heat exposure.

Respiration rate monitoring systems can accurately detect changes associated with muscle tone, chest movement, and exhaled air. An automated long-term respiration rate monitoring system, validated in dairy cows, showed a high correlation with flank movement. Micro-electro-mechanical systems (MEMSs) based on magnetic sensors offer more accurate breathing signals, greater spatial resolutions, and lower measurement errors, making them a promising tool for precise monitoring of respiration rates in cattle.

3.2. Management of Heat Stress in Dairy Cattle

As we already stated above, the optimum temperature for dairy cows ranges between 5 and 25 °C, but during the summer the ambient temperatures go much higher than the maximum comfort limit.

Practical management of heat stress in dairy cows can be grouped into the following four main categories: dietary management, shade, ventilation, and cooling. The most simple and efficient measure regarding dietary management is represented by changing the feeding times during summer. Cows tend to consume more during the night when it is cooler, and during the day they will eat less and in small quantities [13]. It is also recommended to choose feeds that produce less heat during digestion, like grains or proteins, over forages. Attention should be given to avoid digestive disorders such as acidosis and abomasum displacement. Water is also critical during heat stress periods. As temperatures rise, cows will increase their water intake, with consumption rising by 10–20% in hot weather. Thus, it is essential to ensure that yards, buildings, grazing areas, and dispersal areas are adequately equipped with water troughs.

Effective natural ventilation or mechanical solutions can significantly mitigate heat stress. Increasing airflow over cows enhances evaporative heat loss from the skin. Research indicates that airflows as low as 10 km/h can reduce respiration rates in heat-stressed animals by as much as 50%. Installing fans and combining them with water spray can dramatically alleviate heat stress. However, there is conflicting advice regarding the optimal use of water for cooling cows. Some experts recommend wetting cows in the feeding stance with 1.5 L of water over 60 s, followed by 4 min of drying with a 10 km/h airflow. Others suggest a spray cycle of 3.5 L per cow over 3 min, followed by 12 min without water application when temperatures exceed 21 °C.

To prevent long-term economic losses, various cattle selection strategies have been adopted to enhance thermotolerance. These strategies include selecting individuals based on productivity, physiological characteristics, and their response to increased challenges. One proposed selection strategy for achieving thermotolerance involves selecting for reduced milk production. Other strategies include breed crossing and selecting for physiological and cellular traits or a high immune response [16].

Although selecting for lower milk production seems promising for improving heat tolerance, it has significant limitations. A major drawback is that cattle bred for reduced production traits will have lower overall productivity. While heat-tolerant cattle may experience less reduction in yield during heat stress, their total 305-day milk yield is likely to be lower than that of heat-susceptible animals. This approach may not be ideal in countries with seasonal variations, such as Romania, where optimizing year-round productivity is crucial. Furthermore, genome-wide association studies on heat-tolerant animals selected based on reduced milk production have not identified any genes associated with production traits or heat tolerance. This suggests that selecting for lower milk production may not effectively enhance thermotolerance or improve overall genetic resilience to heat stress. Therefore, alternative selection strategies, such as breed crossing or selecting for specific physiological and cellular traits or high immune response, may be more effective in establishing thermotolerance in dairy cattle [17].

Regarding crossbreeding, there are some concerns associated with the capacity of the offspring to resist in cooler climates, so this strategy is probably not ideal for some regions. Another important problem is related to the production capacity of offspring; several studies demonstrated a lower yield capacity [18].

Cellular traits have also been identified as crucial for thermotolerance. One such trait is nitric oxide synthesis, which plays a key role in facilitating vasodilation of the skin during heat stress, aiding in heat dissipation. However, the inclusion of these traits in a selection index is challenging due to the high costs and labor-intensive nature of measuring them, making it difficult to obtain large data sets. Thus, incorporating these cellular traits into a selection index for thermotolerance is currently not feasible [19].

Another promising selection strategy is focusing on high immune responses. Heritability estimates for immune response traits are moderate to high, indicating that these traits can be effectively passed on to subsequent generations. Multiple studies have shown that dairy cattle identified as high immune responders tend to be more thermotolerant than those classified as average or low responders [20]. High immune responders also tend to produce more nitric oxide during heat challenges compared to their average and low counterparts. Importantly, studies have demonstrated no difference in milk production between high-immune responders and other cows. Therefore, selecting for a high immune response in dairy cattle appears to be an ideal, cost-effective strategy for enhancing thermotolerance while maintaining production and minimizing cold stress.

3.3. Physiological and Endocrine System Changes Induced by Heat Stress

Because of physical traits such as coat color, breeds respond differently to heat stress; for example, white cattle are more tolerant to heat stress, being cited in the literature as an increase of about 4.8 °C in black-skinned cattle compared to white cattle that show an increase of about 0.7 °C when subjected to the sun in a directly comparative way. Coat length, thickness, and hair density play crucial roles in the adaptation of animals to tropical climates. Shorter hair, thinner skin, and fewer hair follicles per unit area are directly linked to better adaptability to hot temperatures [21].

The presence of hyperthermia and dehydration has been correlated with increased neuromuscular fatigue, with electrolyte imbalances, acid–base system abnormalities, and renal, cardiac, or respiratory failure being reported. Initially, the increase in heart rate is identified, which induces an increase in peripheral blood flow, thus allowing the transfer of heat and the realization of evaporation mechanisms such as increasing respiratory rate and sweating. To achieve this mechanism, it is necessary to increase water intake and avoid dehydration [16]. Behavioral disorders that may indicate the presence of heat stress are reduced activity and appetite and the inability to maintain the quadrupedal position [11].

Thermal discomfort can be a cause for the dysregulation of molecular and cellular processes, being involved in the disruption of cellular organization by incorrect folding of proteins, thus causing disruption of intercellular transport processes and activation of apoptotic cascades. The disorganization of cellular structures results in increased heat shock proteins (HSPs). The increased expression of HSP mRNA induces inducible HSP. This phenomenon occurs by increasing body temperature that produces the incorrect folding of proteins, thus inducing the release of HSP by dissociating the monomers of heat shock factor 1 that will bind and form a trimer, which is translocated in the nucleus of the cell. The ways of remediation at the protein level are represented by the folding, stopping the aggregation or degradation of the proteins incorrectly folded or denatured in this complex process [16]. Representative proteins for heat shock in ruminants are HSP-70 and HSP-90 [22] (Figure 2).

Changes in the endocrine system activated by heat stress have been demonstrated, for example, the activation of the hypothalamic–pituitary–adrenal (HPA) axis that requires an increase in cortisol and circulating glucose (glucose being a necessary element in the regulation of heat stress in ruminants). Cortisol can induce the sensitivity of the HPA axis with the help of negative feedback proinflammatory cytokines, e.g., interleukin-6.

Heat stress-induced cortisol secretion requires the stimulation of paraventricular neurons to secrete corticotropin-releasing hormone (CRH) that exerts its action on adenenopituitary corticotrophils, stimulating ACTH secretion and inducing cortisol synthesis by the adrenal cortex. Experimentally, it has been shown that the administration of low doses of cortisol during the follicular phase suppresses the production of LH, which demonstrates that the action of cortisol on the hypothalamus suppresses the production of GnRh [23]. Aldosterone is the hormonal product released by the cortex of the adrenal glands with the aim of regulating the balance of minerals and water, i.e., a balance directly affected by thermal stress and which, in severe cases, can induce the stimulation of the renin–angiotensin–aldosterone pathway [24] (Figure 3).

Prolactin is a hormone synthesized in the anterior pituitary gland, which is secreted by mammotrophic cells, with a role in promoting lactation and many other biological processes. Studies show that an increase in prolactin secretion is associated with heat stress.

The common ovarian mechanisms are achieved through an endogenous system that allows for the maintenance of the ovarian temperature at a lower level compared to the rest of the body. This is necessary and important for the preovulatory follicle, which has a lower temperature with values between 0.5 and 1.5 °C. Prolonged heat stress intervenes in the endogenous ovarian cooling system, thus increasing the local temperature and affecting its fertilization capacity [23].

The increased internal temperature of the body directly disrupts endocrine mechanisms and cellular physiology (ovarian cells, germ cells, embryo, etc.). Heat stress acts indirectly by reducing dry food intake, which inhibits the secretion of gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) from the hypothalamic–pituitary system, and directly by altering the uterine environment, causing embryo loss and infertility. Reducing LH levels in cows prevents follicles from maturing and ovulating. GnRH is low and FSH is increased during heat stress [25] (Figure 4).

Follicular estradiol secretion shows low values during heat stress, which disrupts estrus identification, increased gonadotropin, ovulation, gamete transport, and fertilization. Post-ovulation plasma progesterone concentrations are reduced, and this leads to limitations in endometrial function and embryo development. The secretion of progesterone by luteal cells is low during high temperatures; this is also reflected in the lower plasma concentration of progesterone [26].

3.4. Biomarkers of Heat Stress in Livestock

Biomarkers are tools that reflect an interaction between a biological system and a potential hazard, which can be chemical, physical, or biological. These are of several types, i.e., physiological biomarkers, hormonal biomarkers, biochemical biomarkers, enzyme biomarkers, and molecular biomarkers [26].

(a)

Physiological biomarkers: Pulse rate (PR), respiration rate (RR), rectal temperature (RT), skin temperature (ST), and sweating rate (SR) are basic elements in balancing heat stress. These physiological parameters subjected to heat stress present important, essential changes in identifying the exceeding of the thermal comfort threshold, i.e., the respiration rate (RR) value >80 breaths/minute, the increase in body temperature by at least 1 °C, and the increase in pulse rate (PR) are elements described by the literature as specific biomarkers of heat stress. Another physiological element considered important is skin temperature (ST), skin temperature increases by 0.22 °C for each additional degree felt by the animal, and sweating rate (SR) [26].

(b)

Hormonal biomarkers: These are represented by glucocorticoids, thyroid hormones (T3 and T4), catecholamines (epinephrine and norepinephrine), prolactin, and aldosterone. These were discussed previously. Thyroid hormones (triiodothyronine—T3 and thyroxine—T4) play an important role in metabolic adaptation and are true indicators of the effects of heat stress. Serum concentrations of T3 and T4 decrease because of the action of heat stress at the level of the hypothalamic–pituitary axis and at the thyroid level, which causes a decrease in thyrotropin-releasing hormone, thus limiting basal metabolism [24].

(c)

Biochemical biomarkers: Blood glucose, urea, amino acid, protein, free fatty acids, creatinine, haptoglobin, hemoglobin, PCV, and cholesterol are the parameters that are subject to changes under the action of heat stress. In recent years, several adaptation responses have been cited at the blood level, both biochemically and hematologically, such as an increase in the concentration of total hemoglobin (Hb) (increased oxygen requirements), an increase in plasma haptoglobin (this is an acute phase protein used to evaluate the inflammatory response), or an increase in compact cell volume (PCV) [24].

(d)

Enzyme biomarkers: Malondialdehyde, glutathione peroxidase (GPx), superoxide dismutase (SOD), acid phosphatase (AP), aspartate amino transferase (AST), alkaline phosphatase (ALP), and alanine aminotransferase (ALT) are the major enzyme biomarkers involved in heat stressed livestock. Alkaline phosphatase is an important indicator of metabolic activity; its level is low in animals subjected to heat stress. Another metabolic parameter is the plasma concentration of non-esterified fatty acids (NEFA), which is low in the case of dairy cattle subjected to excessive heat [24].

(e)

Molecular biomarkers: The classical heat shock protein (HSP) gene, cytokines, toll-like receptors (TLRs), apoptotic gene, PMEL (premelanosome protein), MC1R (melanocortin 1 receptor), inflammatory gene (NF-κ/nuclear factor kappa B and tissue TNF-α/tumor necrotic factor), microRNAs (miRNAs), genes-associated with thermo-tolerance in ruminant livestock such as superoxide dismutase, nitric oxide synthase, thyroid hormone receptor, and prolactin receptor genes were found to be associated with thermo-tolerance in ruminant livestock. Heat shock protein (HSP) genes HSP70 and HSP90 are increased during exposure to heat stress in ruminants. Inflammatory genes (NF-κB and tissue TNF-α) show an increase directly proportional to the amplification of proinflammatory mediators and systemic inflammatory responses. Skin color genes (PMEL/premelanosome protein and melanocortin 1 MC1R receptor) are modified, and the gene expression of PME and MC1R grows in animals that are raised in environments subject to heat stress.

It has been discovered that miRNA-19a/b and miRNA26a have regulatory roles in innate immunity and thermotolerance in cattle via the targeting of TLR 2 and HSP genes, respectively. The miRNA-27b [27].

3.5. Metabolic Changes and Immune Response

Metabolism in the compensatory attempts uses various hormonal, immunological, or cellular mechanisms that have the role of dissipating body heat. These mechanisms are complex and incompletely researched up to this point.

Other unfavorable consequences of heat stress are represented by the decrease in milk production as well as in the quality of milk. Several studies by Johnson et al. concluded that when body temperature exceeds the comfort threshold, food intake, metabolism, body weight, and production decrease to help compensate for imbalances generated by heat stress [28]. Metabolic heat produced during microbial fermentation accounts for 3 to 8% of the total heat production by cattle [29]. Feed changes have been associated with decreased dry matter intake that can induce a decrease in rumen pH, thus producing rumen acidosis. A decrease in dry matter intake increases the production of rumen flora and causes a change in the appearance of the intestinal villi (they become short), thus decreasing the barrier function for pathogens. As a result of these changes, the immune response is activated.

The cells of the immune system following immunometabolic reorganization processes use aerobic glycolysis to provide energy and produce cytokines, stress proteins, and chemokines, which are essential metabolites in supporting vital functions. Glycolysis is an intense metabolic process identified in dairy cattle subjected to heat stress. Activation of heat shock transcription factor (HSF) and increased heat shock proteins (HSPs) are common compensatory responses to heat stress.

The adaptive immune response under the action of heat stress presents an imbalance between the T-helper 1 (TH-1) and T-helper 2 (TH-2) responses, the shift of responses towards TH-2 [30] being oriented. Cortisol is the body’s main response; it plays a role in binding DNA and induces the stopping of genes that activate TH-1 and the production of proinflammatory cytokines [24], thus resulting in disorders in the formation of the cell-mediated immune response (CMIR) (Figure 5).

Dairy cattle subjected to heat stress show a decrease in lymphocyte proliferation with a role in combating infectious diseases, thus leading to a decrease in the defense mechanism. Neutrophils have a mechanism similar to lymphocytes; the presence of L-selectin on the surface of neutrophils makes it impossible for them to move to the site of action.

Another important pawn of the immune system is the activation of the complement; heat stress is involved in disrupting the coding of the various components of the complement system.

Other metabolic processes cited during heat stress are the suppression or increase in fatty acid oxidation in lactating cattle, an aspect incompletely researched at this time. Another process cited is the presence of an increase in ketone bodies, an aspect identified due to the decrease in the level of carbohydrates in the ration [16]. The daily intake of water is important in regulating body temperature. It is available in three forms, i.e., drinking water, water resulting from feed, and metabolic water. Increased water consumption is correlated with increased urine volume, respiratory evaporation, or heat loss through evaporation [31].

It has been shown that cattle with high yields are more prone to sensitivity and subjection to heat stress, sometimes this aspect being directly related to their breed; thus, heat stress prevents dairy cattle from fully expressing their genetic potential for milk production and affects milk composition.

The mammary secretory function depends on the number of mammary epithelial cells and their secretory activity. It has been demonstrated that cattle subjected to heat stress experience cellular apoptosis and disruption of physiological activity, leading to a subsequent decrease in both the quantity and quality of milk produced. The decrease in the concentrations of milk proteins and casein (α-casein, β-casein, and κ-casein) and the redistribution of amino acids to achieve gluconeogenesis are important metabolic elements in decreasing the negative effects of heat stress [32].

Mild to severe heat stress can increase metabolic maintenance requirements by 7 to 25%, decrease conception rate by up to 20–30%, decrease estrous manifestations, and decrease BCS [33].

Lactating cows show increased levels of plasma insulin, decreased blood glucose, increased levels of plasma urea nitrogen, increased gluconeogenesis and amino acid intake, increased liver glucose production levels, increased blood creatinine, etc. Short-term heat stress can trigger lipolysis in adipose tissue and proteolysis in skeletal muscle, while long-term heat stress inhibits lipolysis in adipose tissue and exacerbates proteolysis in skeletal muscle.

3.6. Reproduction and Fertility

Seasonal high temperatures are associated with poor reproductive success in dairy cows. Heat stress during summer disturbs reproductive activity of dairy cattle in all stages, starting from breeding point to late in gestation. It is well recognized that during the hot season most cows do not express estrus behavior even if ovulation occurs [34]. Heat stress causes a decrease in the production of clear, stringy mucus discharge and a decrease in mounting behavior, which are both reliable signs of estrus [35]. This happened because heat stress induces a decrease in peripheral estradiol-17b concentrations during estrus [36]. Several studies conducted demonstrate that the dominant follicular fluid of animals subjected to heat stress contained much more androstenedione and significantly less estradiol-17b [36] due to impaired steroidogenic potential of follicular granulosa cells. It is clearly demonstrated that the heat stress induces oxidative stress of granulosa cells, demonstrated by the increased intracellular reactive oxygen species accumulation [37]. It seems the reduction capacity of estradiol production by granulosa cells can be attributed to diminished expression of gonadotropin receptors [38] or the downregulation of genes related to steroidogenesis, such as CYP11A1 and STAR [39].

Follicular development in cattle occurs in wave-like patterns, consisting of two to four follicular waves. The main factors controlling ovarian activity and follicular wave development are Gn-RH from the hypothalamus and anterior gonadotropins (FSH and LH). The effects of heat stress on gonadotropins are controversial [40] and strongly related to other hormones and metabolites. Interestingly, heat stress facilitates the activation of the primordial follicles, which is likely attributed to enhanced and accelerated metabolism [41]. Heat stress suppresses the LH pulse amplitude and frequency, compromising the maturation of dominant follicles [26]. A lower LH surge and lower LH tonic levels during heat stress periods were documented, which impair ovulation and functional CL formation, leading to a low progesterone level [26]. Anyway, short-term exposure to heat stress either had no effect on plasma concentrations of progesterone [42] or caused an increase [43,44]. Long-term exposure to heat stress may lead to reduced progesterone concentrations [45]. Moreover, due to a decreased level of plasma inhibin and the increased availability of preantral follicles for activation and development, a larger number of follicles may grow in the ovary, which may cause double ovulation and, subsequently, twin calving during the summer season [40,42].

The development pattern of ovarian follicles, along with hormonal imbalances in the HPA axis involving cortisol, significantly impacts ovarian cyclicity and, more notably, oocyte quality. In vitro studies show that high temperatures cause functional and structural defects in maturing oocytes, including incomplete migration of cortical granules, impaired mitochondrial distribution, and increased ROS accumulation [46,47]. Increased oxidation will trigger apoptotic phenomena associated with increased DNA fragmentation, impaired distribution and function of mitochondrial and cortical granules, and disrupt microfilament and microtubule rearrangement [48,49], causing a reduced size of meiotic spindle with reduced oocyte maturation [45]. This will lead to several complications, including issues with the fertilization process. As is shown in several in vitro studies, the heat-stressed bovine mature oocytes exert low protein synthesis, fertilization rate, and subsequent developmental competence [50,51]. Conception rates have been shown to be affected both before and after breeding during the hot season, with the greatest impact being before breeding [52].

Despite all these negative influences, pregnancy can be obtained even in summer, the hottest month. However, heat stress may affect or influence in a negative way embryos during early pregnancy. At the time the embryonic genome becomes activated, which takes place after the first stage of cleavage, increased transcription activity and protein synthesis are observed [53,54]. At this stage, several heat shock proteins (HSPs) and antioxidant enzymes are overexpressed, strengthening the defense molecular mechanisms of thermotolerance in the developing embryo. Even if the embryo gains some certain degree of resistance to a minor change in temperature, sustained exposure to higher temperatures can reduce the number and quality of embryos, fertilization, implantation, and successful pregnancy rates [55]. These modifications appear as a result of increased concentrations of ROS such as hydrogen peroxide and superoxide anion, as several studies demonstrated on cultured bovine embryos, which reduced embryo quality through apoptosis [56]. This sensitivity is evident in the higher incidence of late embryonic losses during the summer, which can affect up to 40% of confirmed conceptions [57].

Heat stress during late pregnancy does not affect only the cow but exerts a negative impact on the calf in utero. Many in vivo studies have demonstrated a lower birth weight of calves from females who experience heat stress late in gestation [58,59,60]. This happened since during heat stress periods, females will reduce dry matter intake trying to reduce the metabolic heat load, resulting in fewer nutrients provided for the calves in the last few months of pregnancy when the growth rate of the calf is very high [61]. Placental growth and function have also been shown to be altered during heat stress [58,61], which can explain the low birth weight of calves during heat stress periods. Similarly, retarded fetal growth was observed in lambs born from sheep exposed to heat stress during late gestation due to suppressed placental development, with a reduced cotyledonary mass and decreased mid-uterine artery blood flow [62].

A decreased gestation length has been reported after exposure to heat stress during gestation [61,62]. It seems the gestation length is reduced up to 4 days, which shortens the time the calf grows in utero [62].

Heat stress in utero affects survival rates, leading to an increased number of stillborn calves. Exposure of dairy cows to heat stress during late gestation negatively impacts the postnatal immune status and performance of calves. It increases intestinal apoptosis, reducing IgG absorption and impairing passive immune competence [63].

Heat stress seems to impact the calf even after birth. Calves exposed to heat stress in utero have reduced consumption of calf starter up to weaning, have reduced growth up to 12 months of age, and seem to have reduced reproductive performances, requiring an increased number of services to become pregnant [58,59,60].

3.7. The Effects of Thermal Stress on the Mammary Gland

Dairy cattle that experience heat stress during late pregnancy typically experience lower milk yield in the subsequent lactation [61]. This is associated with increased PRL serum concentration associated with heat stress, as we show above. Prolactin is an important hormone that supports mammogenesis and lactogenesis, but the increase in circulating PRL concentration will determine a decrease in the expression of PRL receptor genes in the mammary gland, liver, and lymphocytes [62]. As a result, this will lead to decreased function and growth of the mammary gland, impairing lactogenesis and reducing milk production in the subsequent lactation after calving [63]. Reduced cell proliferation during heat stress periods is the main mechanism that reduces mammary growth and impairs lactation performance [64].

Research has shown that dairy cattle respond differently both physiologically and productively based on the type and duration of heat stress they endure. Lactating cows produce the highest milk yields within an ideal temperature range of 5 to 25 °C [65]. Heat stress increases oxidative stress, which changes mammary secretory tissue metabolic and molecular activity, decreasing cellular efficiency for synthesizing milk components [66] and changing milk composition [67].

3.8. Production Decline Analysis

Heat stress can significantly drive up production costs in the dairy industry. The THI threshold at which heat stress occurs is the point at which the decrease in milk production is identified. It is correlated with breed and comprises different thresholds that vary depending on location or production level [16].

Several studies carried out in the field of animal production outline the decrease in production in breeds such as Holstein by up to 10% compared to the autumn or spring season [28]. Some studies claim that for every 10 kg/day of weight gain, the heat stress threshold decreases by 5 °C [68], thus milk production decreases by values between 0.158 kg/day and 0.335 kg/day depending on the productive characteristics [69].

Reducing DMI during heat stress produces a significant decrease in milk production; for example, decreasing DMI to a level of approximately 40% leads to a decrease in between 23 and 53% compared to animals that have not been subjected to heat stress [29,70].

As a result of the protein imbalances discussed, biosynthesis and transport to the mammary gland decrease, which leads to an increase in the energy requirement in supporting cells in milk production. The reduction in protein processes can also be a cause for a decrease in milk quality, as essential amino acids are identified in circulation and used to provide maintenance energy [16]. Heat stress has been shown to have the greatest impact on milk composition during the first 60 days of lactation [29]. Garner et al. [69] have shown that cows that are exposed to heat for a long time produce milk with a composition up to 49% lower in lactose and protein. Heat stress is usually measured in dairy cattle via the temperature–humidity index (THI).

Additionally, milk yield in Romania has declined by 7.6% over the analyzed interval, dropping from 3643.8 kg per cow in 2013 to 3367 kg per cow in 2022 [70].

We used physiological and behavioral data collected in Romania and Europe to analyze milk yield trends. Currently, Romania is disadvantaged, with an average milk yield of 3447 L per cow, significantly lower than the EU average of 6085 L [71]. Heat stress further exacerbates this issue, potentially reducing milk yield by about 2.8% compared to the current European yield, leading to estimated financial losses of around 5.4% of farmers’ monthly income during the summer season [72].

In this context, it can be concluded that Romanian dairy farms are vulnerable, and milk production is decreasing considerably compared to neighboring countries.

4. Conclusions

This literature review highlights the physiological and pathophysiological changes induced by heat stress in dairy cattle, outlining the negative secondary economic effects. This approach involves the analysis of cattle from a physiological, pathophysiological, and productive point of view, so we choose to study metabolic, behavioral, and productive changes as the effects of physiological and pathophysiological adaptation to heat stress.

This literature review discusses the modes of action of heat stress and the physiological or pathophysiological mechanisms that induce important economic losses. Finally, we chose to give importance to clinical signs suggesting the presence of heat stress and the mechanism of installation and selection of individuals with increased tolerance to temperature variations.

5. Future Directions

Heat stress is a serious problem for dairy cows that persists due to the continuous climate changes in the last decade. Heat stress leads to important changes that affect the welfare of cattle and cause increased economic losses globally. These effects indicate the need for and implementation of viable strategies for the selection or production of cattle that show increased tolerance for the important thermal variations in which the temperature increase above the tolerance limit occurs over long periods of time. To the same extent, we believe that selection programs should take into account the climatological characteristics of each country or region, thus making the selection avoid individuals susceptible to intolerance of low or high temperatures that could induce significant economic losses secondarily.

Data from the literature provide relatively little information about the selection programs for thermosensitive individuals. The information also focuses on identifying changes in general health and stating general measures that seek to counteract the effects of heat stress on the health and yields of dairy cows.

In our opinion, the approach must have a direction focused on the possibility of adapting and selecting cattle breeds that show increased tolerance for sudden temperature variations without compromising on national management adaptation mechanisms.