Chapter 52 Divakar J. Ambrose Livestock Research Branch, Alberta Agriculture and Rural Development and University of Alberta, Edmonton, Alberta, Canada Postpartum anestrus refers to a condition where cows have not been observed or reported in estrus for several weeks after calving, often to the end of the voluntary (elective) waiting period, in dairy cattle. While a short period of ovarian inactivity during the immediate postpartum period is normal, extended anestrus in nonsuckled cattle such as dairy cows could have negative ramifications on the timely reestablishment of pregnancy.1–4 Postpartum anestrus has been recognized as a problem by animal scientists for several decades. According to one source,5 anestrus in cattle was reported first as a reproductive problem back in the 1920s.6 There has been significant interest in the past two to three decades in the understanding and management of postpartum anestrus, both in beef and dairy cows.5–13 Nevertheless, postpartum anestrus continues to be a challenge to dairy practitioners and farmers alike. This chapter will focus primarily on the problem of postpartum anestrus and its management in dairy cattle, although references to the condition in beef cattle will be made where appropriate. The modern dairy cow is an important livestock species with a remarkable ability to produce tens of thousands of liters of milk during her lifetime. Understandably, the profitability of dairy farming is closely integrated with the reproductive success of the dairy cow. However, suboptimal fertility of the modern dairy cow is a problem that afflicts the dairy industry worldwide,14–18 with reproductive failure often being the primary reason for culling dairy cows.19–21 While the reasons for declining fertility in dairy cattle will continue to be debated through the years to come, it is important to bear in mind that the modern dairy cow is physiologically quite different from her counterparts of past decades,16 calling for new and improved strategies of reproductive management to maintain or enhance reproductive success. An extended period of postpartum anestrus is one among the many factors contributing to poor reproductive efficiency in dairy cattle. Rajala-Schultz and Gröhn22 showed that if a cow had not been inseminated at all, her risk of culling was ten times higher than if she was inseminated at least once. While a deliberate managerial decision to not breed a cow, due to past history, may have directly contributed to this increased culling risk, anestrus could also have increased the risk, emphasizing the importance of detecting cows in estrus and having them bred in a timely manner. The prevalence of postpartum anestrus in dairy cattle is herd-specific and varies widely from one herd to another. However, typical prevalence rates at the end of the elective waiting period (60–80 days after calving) are in the range 10–30%,23–28 whereas higher rates of up to 59% have been reported in individual herds.16,25,27 In a Canadian study involving 23 herds, milk progesterone concentrations were measured twice weekly in 637 cows to determine the onset of cyclicity, starting approximately 7 days after calving up to 120 days after calving.28 The overall interval from calving to first rise in progesterone, indicative of an ovulation, was 32.0 ± 0.7 days. The cumulative percentages of cows initiating cyclicity by 3, 6, 9 and more than 9 weeks after calving are shown in Figure 52.1. Although these findings may suggest that postpartum anestrus is not necessarily a huge problem because 90% of the cows had initiated cyclicity by 9 weeks, which is the typical end of the elective waiting period, it is important to note that cows that initiated cyclicity during the early postpartum period had higher conception rates at first service (Figure 52.2). Similar findings have been reported by others.1,2,4,24,28 The biggest impact of postpartum anestrus is the extension of the interval from calving to conception, which consequently impacts the calving interval. Whereas high-producing dairy cows that fail to return to estrus and conceive soon after the end of voluntary waiting period may continue to remain profitable for a period of time, cows with lower production that remain acyclic for an extended period, resulting in delayed conception, are often unprofitable and become potential targets for culling. During gestation, circulating progesterone and estrogen concentrations remain high, exerting a suppressive effect on the hypothalamic–pituitary axis.29 Although peripheral progesterone concentrations in late gestation are not much higher than that of mid-luteal or early gestational periods,30,31 circulating estrogens progressively increase starting at about 60 days of gestation reaching 50 to 1000-fold higher concentrations in the days immediately preceding parturition.30,32 The sustained long exposure to high concentrations of estradiol, either by itself or in tandem with progesterone, inhibits hypothalamic gonadotropin-releasing hormone (GnRH) secretion, which negatively affects the synthesis of luteinizing hormone (LH) leading to a gradual depletion of pituitary LH reserves. Although the mechanisms for release of LH from the anterior pituitary gland remain intact and functional throughout pregnancy,29 the absence of pulsatile GnRH secretion from the hypothalamus is what appears to negatively impact LH production. Unlike LH, changes in the concentrations of follicle stimulating hormone (FSH) during late gestation are less remarkable. While mean FSH concentrations do not differ between prepartum and postpartum periods,30,33 the recurrent rise and fall (surge) of FSH that typically occurs every few days in cyclic and pregnant cows is largely absent30 or slowed down33 during the last weeks preceding parturition. Consequently, the associated follicular wave emergence is also absent during the last 30 days before parturition.33 Whereas it is possible to restore the pulsatile release of LH under experimental conditions by administering low-dose GnRH injections at frequent intervals (1–2 hours), not all cows respond to such treatment. Because of the inconsistent response to such an approach, it is believed that the inhibition of GnRH secretion is perhaps not the only mechanism involved in anestrus.5 As parturition approaches there is a gradual decrease in progesterone concentrations. In contrast, estrogen concentrations keep rising and peak by doubling during the last 24 hours prior to parturition. Since almost all circulating estrogens are of placental origin, their concentrations plummet sharply after expulsion of the conceptus reaching basal levels within 1 day after calving.32 In the absence of progesterone and estradiol in the immediate postpartum period, the hypothalamic–pituitary axis is “liberated” from the suppressive effects of these steroids, resulting in the restoration of normal function of the GnRH pulse generator and the resultant pulsatile release of GnRH, which acts on the pituitary to restore a normal pattern of FSH release. Normal FSH surges resume within 3 days after calving, triggering the emergence of a follicular wave.30 Whereas early stages of follicle development are gonadotropin independent, FSH support is required for the growth of follicles from 4 to 9 mm and LH pulses are indispensable for continued growth of follicles beyond 9 mm in diameter.34,35 During the early postpartum period the LH pulse frequency remains very low, generally less than one pulse every 4 hours, which later increases to about one to two pulses per hour as GnRH pulsatility increases. The restoration of pituitary function and reaccumulation of LH could take up to 3 weeks or longer depending on several factors. Thus, when conditions are optimal for pituitary LH reserves to be replenished, normal LH pulsatility is restored leading to the growth and establishment of dominant follicles capable of producing greater quantities of estradiol. A high concentration of estradiol from the dominant follicle is essential to trigger an LH surge, which is critical for the first ovulation to occur. Although the first ovulation signals resumption of cyclicity, not all cows would resume normal ovarian cycles following the first ovulation and could relapse back into anestrus.36 If cows are challenged with either exogenous GnRH or estradiol during the early postpartum period, not only is LH release greatly diminished due to lack of pituitary LH reserves, but also its bioactivity is lowered.5 The fate of the first dominant follicle in the postpartum cow is determined by the pulsatile LH support it receives and by its own steroidogenic capacity to produce estradiol. Depending on these factors, the first dominant follicle may (i) ovulate and form a corpus luteum (CL); (ii) become anovulatory, possibly developing into a cystic follicle; or (iii) regress, making way for a new dominant follicle.37,38 Postpartum anestrus can be classified into different types based on either ovarian follicle dynamics or progesterone profiles. The classification of anovulatory conditions in cattle based on three functionally critical follicular diameters relating to emergence (~4 mm), deviation (~9 mm), and ovulation (10–20 mm) has been proposed.39 With the above classification as the basis, four types of anestrus, types I to IV, were described by Peter et al.13 (Figure 52.3). In type I anestrus, there is growth of follicles up to emergence but no deviation occurs resulting in lack of selection of a dominant follicle. This type of anestrus is presumed due to extreme malnutrition, which could exert a negative effect on FSH production suppressing follicular growth, although other factors could also be involved. Ovaries under this type may be described as either “inactive” or “smooth” as a reference to the lack of palpable ovarian structures during reproductive examinations per rectum. An Israeli study40 from the 1980s reported an incidence of 8.5% inactive ovaries from 7751 lactations. While type I anestrus is not widely seen in dairy cattle of developed countries, this type of anestrus could be more prevalent in regions of the world where balanced energy-dense rations are unavailable to dairy cattle. In type II anestrus both follicular deviation and growth occur, followed by regression, in some cases, after a follicle attained dominance. Regression of a dominant follicle is usually followed by the emergence of a new follicular wave, 2–3 days later. In this type of anestrus, there may be sequential emergence of follicular waves prior to the eventual occurrence of the first ovulation. Up to nine waves of follicular growth have been reported in one study.41 In type III anestrus, deviation, growth, and establishment of a dominant follicle takes place, but the dominant follicle fails to ovulate, becoming a persistent structure which may either linger as an anovular follicle or continue to grow and develop into a cystic follicle. Anovular follicles are considered different from cystic follicles because in cows with the latter condition there is disruption of the feedback mechanisms in the hypothalamic–pituitary axis.42 The secretory pattern of LH in cows with cystic ovarian follicle is quite different from that in normal cyclic cows in that mean concentrations of LH, frequency of LH pulses, and amplitude of LH pulses are all higher;43 in addition, in cows with an actively growing cystic follicle, the estradiol concentration is also significantly higher.44 A cystic follicle that is growing actively usually exerts dominance, suppressing the growth of other follicles. Retrospective analysis of data from twice-weekly ultrasonography, from 7 to 35 days after calving, on eight lactating dairy cows that developed cystic ovarian follicles, a first-wave dominant follicle became cystic in seven cows, and a second-wave dominant follicle became cystic in one cow. No other follicle greater than about 5–6 mm diameter was detected on either ovary of cows until the cystic follicle turned over. In five cows, the cyst persisted until (possibly beyond) day 35; in two cows, the initial cystic follicle was replaced by another one; in one cow two follicles from the second follicular wave became dominant around day 30 at which time the original cyst had regressed to below 20 mm diameter giving way for both dominant follicles to ovulate (Divakar J. Ambrose, personal observations). In type IV anestrus, a dominant follicle ovulates and forms a CL, but the luteal phase is prolonged due to the absence of timely luteolysis followed by CL regression. Aberrant follicular growth patterns resulting in the absence of an estrogenic dominant follicle at the ideal time to trigger luteolysis could be a reason for this condition of persistent CL.39 Cows can also be classified into different categories of anestrus based on progesterone measured in milk or blood at least on a twice-weekly basis. Using twice-weekly measurement of progesterone in milk fat on 334 dairy cows from six herds, Opsomer et al.45 reported that 51% of the cows had a normal progesterone profile with the first rise in progesterone occurring before 50 days after calving, followed by regular cyclicity. Among the remaining population, 21.5% of the cows had delayed cyclicity (anestrus for the first 50 days after calving, characterized by consistently low progesterone during that entire period), 21.5% had prolonged luteal phase (progesterone remained elevated for >20 days without a preceding insemination), 4% had cessation of cyclicity (normal cycles interrupted by at least 14 days of consistently low progesterone concentrations), 0.5% had short luteal phases (characterized by more than one luteal phase, excluding the first luteal phase, that was shorter than 10 days’ duration), and 1.5% of the cows had irregular progesterone profiles (atypical profiles, that did not belong to any of the previously described categories). The causes of postpartum anestrus in cattle are often multifactorial,5,8,10,12,13,38,46–50 but can be broadly categorized into physiological, nutritional, managerial, environmental, and pathological as detailed in Table 52.1. Among the numerous potential contributors, suckling and nutrition (negative energy balance) are considered the most important. Table 52.1 Direct and indirect causes of anestrus in cattle. Note: This list should not be deemed complete and the references are representative citations only. Suckling is a major contributor to anestrus in beef cattle,46 but it is generally not considered a cause for anestrus in dairy cattle because of the prevailing industry practice of separating dairy calves from the dam soon after birth. However, under experimental conditions when identical twin pairs of dairy cows were assigned to either suckling by multiple calves or twice-daily machine milking, the suckled cows had a 5–9 week longer interval to first estrus after calving than their machine-milked twins. Basal plasma concentrations of LH did not differ between suckled and machine-milked twins, yet GnRH-induced LH release increased progressively in machine-milked cows from weeks 0 to 6 after calving, and the LH response at 2 weeks after calving was significantly higher in machine-milked cows than in their suckled twins.73 Estradiol-17β-induced LH release within 24 hours after treatment was delayed by up to 6 weeks in suckled cows compared with their machine-milked twins, indicating that the response of the hypothalamic–pituitary axis to both GnRH and estradiol-17β is impaired by suckling. In another study,74 suckled dairy cows had lower mean LH concentrations than nonsuckled controls on day 13 after calving. This decrease resulted from a 60% reduction in the frequency and a 40% reduction in the amplitude of LH pulses. These authors concluded that decreased frequency and amplitude of episodic LH secretion and reduced capacity of pituitaries to respond to GnRH may account for suckling-induced inhibition of postpartum ovulation. For further reading on the effects of suckling on postpartum anestrus in cattle, please refer to reviews on the topic46,49,50 and Chapter 23. Inadequate consumption of dry matter (i.e., energy) resulting in negative energy balance is an important contributing factor to anestrus in dairy cattle.11,38,48 Soon after calving, the energy needs of the newly lactating cow increase dramatically due to the higher energy requirements associated with milk production, pushing the cow into a catabolic metabolism. Energy balance is the net result of energy intake minus energy expended for maintenance, growth, and milk yield. Although dairy cows rarely enter into a state of negative energy balance during dry period, except in the immediate prepartum period when dry matter intake declines, most lactating dairy cows are unable to meet their energy demands after calving and invariably become energy deficient. Physical fill in the rumen is one of the factors limiting maximum dry matter intake in early postpartum dairy cows. Even if dry matter intake is maximized, cows selected for high milk production (e.g., North American Holstein) selectively use all available nutrients for milk production at the expense of body condition.65 Thus nutrient partitioning prevents cows from ending the catabolic state because all the available glucose is preferentially used up for milk synthesis.75 Despite the advances made in the understanding of dairy cow nutrition and the availability of high-precision ration-balancing software, meeting all the energy needs of a lactating dairy cow continues to remain a challenge, placing cows in a state of negative energy balance that extends for 10–12 weeks into the postpartum period.11 Dairy cows that are in negative energy balance have lower blood concentrations of insulin and insulin-like growth factor (IGF)-1. Low circulating concentrations of IGF-1 reduce the negative feedback on growth hormone (GH), resulting in an increase in GH concentrations. Increased GH increases liver gluconeogenesis and promotes lipolysis (mobilization of adipose tissue) resulting in the release of nonesterified fatty acids (NEFAs). High concentrations of GH and NEFA antagonize insulin action, creating a state of insulin resistance in postpartum dairy cows,64,75 which diminishes glucose utilization by nonmammary tissues, conserving glucose for milk synthesis. Negative energy balance is strongly associated with the postpartum anovulatory period through decreased LH pulse frequency and low concentrations of blood glucose, insulin, and IGF-1 that collectively limit estrogen production by dominant follicles11 which is essential for the LH surge, thereby delaying ovulations. High stocking density that increases competition for feed, poor stall design that discourage cows from getting up frequently to eat, physical barriers that limit free and continuous access to feed, infrequent feed push-ups, excessive sorting by cows that get to the feed first, and inadequate hoof care leading to high prevalence of lameness are all indirect causes that can reduce dry matter intake. Furthermore, social hierarchy situations where younger or subordinate animals are intimidated by herdmates, stray voltage, slippery footing, and other deterrents can all dissuade cows from comfortably accessing feed, limiting dry matter intake and predisposing cows to enter a state of negative energy balance. Unobserved estrus is often a major contributor to anestrus as many of the cows considered anestrous could in fact be cycling normally, yet never seen or reported in estrus. There are two categories of animals. Both categories of cows may ovulate spontaneously and develop a CL; however, because they were never seen in estrus, they are falsely categorized as “anestrus.” Performing more frequent visual detection of estrus (say three to four daily periods of dedicated surveillance) and observing for secondary signs of estrus such as chin-resting, vulva sniffing, licking, tailgating, and partial attempts to mount, rather than strictly for “standing estrus,” will increase the probability of detecting estrus in these cows. The first ovulation after calving is rarely preceded by overt estrous behavior; only 10–13% of dairy cows reportedly exhibit standing estrus prior to the first ovulation,36,76 although this proportion increases significantly in the second and third ovulatory cycles (Figure 52.4). The level of milk production could also influence the proportion of cows detected in standing estrus at first ovulation,36,76,77 with a higher proportion of low-producing cows detected in standing estrus at first ovulation (Figure 52.5).
Postpartum Anestrus and its Management in Dairy Cattle
Introduction
Fertility of the high-producing dairy cow
Prevalence and implications of postpartum anestrus
Physiological basis for postpartum anestrus and resumption of cyclicity
Endocrine events leading to anestrus
Endocrine events leading to the resumption of cyclicity
Fate of the first dominant follicle
Classification of postpartum anestrus
Categorizing anestrus based on ovarian follicular dynamics
Categorizing anestrus based on progesterone profiles
Factors contributing to postpartum anestrus
Causal factor
Comment
Physiological
Suckling
Suckling suppresses episodic LH secretion, thereby delaying ovulation.46,49,51 Suckling is a major contributor to postpartum anestrus in beef cattle, but not so in dairy cattle because dairy calves are usually separated from the dam soon after birth
Parity
Parity as a risk factor for anestrus has been reported in numerous studies.45,47,52 Most reports suggest that first-parity cows are at a higher risk of anestrus due to delayed first ovulation. Multiparous cows, particularly those with four or more calvings, are reportedly at a significantly higher risk for anestrus due to prolonged luteal phases. The reason may be that with increasing parity the uterus takes more time to return to its pregravid size, thereby increasing the risk of pyometra and persistent CL45
Milk yield
Although high milk production has been identified as a risk factor for anestrus by some researchers,27,52,53 others have not found such an association. In one study,27 the probability of anovulation decreased by 2% for every 100-kg increase in the first 305-day mature equivalent milk projection between 5000 and 9500 kg, and the risk of anovulation did not change as first 305-day mature-equivalent milk increased above 9500 kg. Similarly, another large study52 found that cows with lower daily average milk yield in the first 90 days postpartum (32.1 vs. 39.1, 43.6, 50.0 kg/day) were at higher risk for anestrus. It is unlikely that high milk production itself is a cause for anestrus; however, the inability to meet energy requirements leading to negative energy balance, a common problem in lactating dairy cows, is the most likely reason
Ratio of increase in milk yield
The ratio of increase in milk yield from the first week postpartum to the week when milk yield reached its peak is reportedly smaller in ovular than in anovular cows54
Social or chemical cues
In beef cattle, the interval from calving to resumption of cyclicity is significantly reduced by the presence of bulls.55 In one study the exposure of bulls in the early postpartum period had an acute effect on LH release in anestrous dairy cows.56 Likewise, the presence of other estrous females or exposure to cervical mucus collected from estrous cows can also shorten the duration of postpartum anestrus,57 particularly in cows with extended anestrous periods
Breed
The influence of breed or type (genetic) differences on the interval from calving to commencement of luteal activity has been reported, mainly in beef cattle and crossbreds47,58
Nutritional
Malnutrition
Severe feed restriction will induce anestrus in cattle. In one study,59 nonlactating beef cows placed on a restricted diet formulated for 1% of body weight loss each week became anestrous after 26 weeks and lost 24% of their initial body weight. Estrous cycles resumed about 9 weeks after cows were returned to a diet that was 160% of the maintenance diet given to control cows. Anestrus was associated with a decrease in the frequency of LH pulses
Negative energy balance
Cows in negative energy balance are at a very high risk of anestrus and delayed onset of cyclicity.11 Elevated circulating concentrations of nonesterified fatty acids are associated with adipose tissue mobilization and indicative of negative energy balance
Body condition and rate of loss of body condition
A body condition score (BCS) of less than 3.0 on a 1–5 scale is commonly an indicator of negative energy balance.45,52 Cows with low BCS are more likely to be anestrous and it has been reported that the influence of body condition on the duration of postpartum anestrous period is mediated through differences in LH pulse frequency.60 Cyclic cows with low BCS tend to have poor conception rates and higher embryonic losses.52,61 A higher rate of body condition loss has been associated with extended intervals from calving to resumption of cyclicity or first service
Managerial
Length of previous dry period
Cows having a dry period longer than 77 days were almost three times more at risk of anestrus and delayed ovulation.45 In contrast, the interval from calving to first ovulation in cows given no dry period (fed a high-energy diet continuously) compared to those given a 56-day dry period (fed a low-energy diet from 56 to 29 days prepartum followed by a moderate-energy diet for the last 28 days) was significantly shorter (13.2 vs. 31.9 days)62,63
Increased milking frequency
Increasing the frequency of milking from twice to three or four times daily lengthens the interval from calving to first ovulation by less than a week. When milking frequency is increased from three to six times daily, the interval to first ovulation is lengthened, but still not to the same extent as that of frequent suckling.49 Therefore, increased milking frequency is only a minor contributor to anestrus
Efficiency of estrus detection
Unobserved estrus due to poor estrus detection efficiency can frequently contribute to anestrus,28 exacerbating the severity of the condition
Feed and feeding management
Inadequate dry matter intake is one of major reasons for cows entering a state of negative energy balance.38,64,65 Maximizing dry matter intake through particle size management, frequency of feed delivery (more than one feed), grouping cows by parity/production levels/social order, feed bunk management (e.g., frequent push-ups), discouraging sorting behavior by adding water, avoiding overstocking, etc. are some examples of strategies to improve dry matter intake, thereby reducing negative energy balance
Environmental
Calving season
Cows calving in the winter have delayed resumption of estrous cycles compared with those calving in the summer.7,27,45 While some of the variations attributed to season are likely due to seasonal differences in management, photoperiod does seem to play a role in the regulation of postpartum cyclicity
Weather
Under extreme hot and humid conditions, cows have reduced expression of estrus,7 which contributes to an increase in anestrus due to sub-estrus and silent estrus
Social hierarchy
Social hierarchy (e.g., presence of dominant cows) could be a factor that has detrimental effects on feed intake, particularly in overstocked barns. It is not uncommon to see “bullying” among cows. The subordinate or the “bullied” cows frequently end up eating leftover feed which may be of poor quality as it is likely to have been sorted through. Such cows are at higher risk for negative energy balance, thus anestrus
Housing type
Cows under intensive housing systems compared with those on pasture have a higher risk of anestrus. Tie-stalled cows are more likely to be in anestrus than other types of housing;47 one explanation is that tie-stalled cows have few opportunities to form sexually active groups, limiting overt behavioral signs of estrus
Stocking density
Stocking density could have a significant impact on access to feed bunks, negatively affecting feed intake, particularly where cows of different pecking order are mingled in the same feeding group
Stall design (cow comfort)
Poorly designed stalls (e.g., lack of lunge space) would limit the frequency of accessing feed bunk/manger, negatively affecting dry matter intake, predisposing cows to negative energy balance and consequently anestrus
Stray voltage
Few studies have examined the effects of stray voltage on reproductive function in cattle. Although no direct evidence of stray voltage on impairment of ovarian function could be found, it is a potential contributor to the problem of anestrus as bothersome stray voltage in and around the feeding area could be a deterrent to feed intake
Pathological
Uterine inflammation
Cows with acute forms of metritis and those with severe bacterial contamination of the uterus have delayed resumption of cyclic ovarian activity.45,66 The mean interval from calving to first ovulation was longer (45 vs. 32 days) in cows that were determined to have uterine inflammation (based on higher proportion of polymorphonuclear, or PMN, cells at endometrial cytology performed on day 25 postpartum) compared with cows with no uterine inflammation.67 The cumulative pregnancy (%) at 270 days postpartum tended to be lower in cows with high PMN (58 vs. 80) than in those with low PMN counts
Persistent corpus luteum
Cows with uterine infections accompanied by abnormal vaginal discharge are at much higher risk for anestrus due to prolonged luteal cycles.45 However, prolonged luteal phases of >30 days’ duration have been reported in cows that were not previously inseminated, even in the absence of any uterine infections15,68
Cystic ovarian follicle (COF)
Though not strictly a pathological condition, cows diagnosed with COF are often anestrous and anovulatory.69 The precise etiology of COF is still not fully understood, but an aberration in LH secretory pattern is believed to trigger the formation of COF; cows with active COF have increased LH pulsatility, which is essential for continued growth of the cyst42,70
Calving disorders
Dystocia, twinning, and retained placenta could predispose cows to anestrus27,45
Metabolic disorders
Ketosis and displaced abomasum have been associated with delayed cyclicity and anovulation,27,45 particularly in cows with subclinical ketosis during the first week postpartum27
Lameness
The increased risk of anestrus associated with lameness has been reported by many studies45,71,72
Mastitis
Mastitis by itself has been identified as a risk factor for anestrus.45 Cows that suffered lameness and mastitis, or lameness and another severe stressor, were at much greater risk for delayed onset of cyclicity72 than cows with mastitis alone
Other disease
Cows that developed pneumonia during the first month after calving were 5.4 times more at risk for delayed resumption of ovarian activity.45 Numerous other types of systemic illnesses can contribute to the condition as sick cows will have reduced dry matter intake, increasing their risk to enter a state of negative energy balance, thereby anestrus
Suckling
Nutrition
Unobserved estrus or silent estrus