CSIRO PUBLISHING
Review
Reproduction, Fertility and Development, 2015, 27, 872–879 http://dx.doi.org/10.1071/RD14390
Not just a number: effect of age on fertility, pregnancy and offspring vigour in thoroughbred brood-mares Charles F. Scoggin Claiborne Farm, PO Box 150, Paris, KY 40362, USA. Email: [email protected]
Abstract. Advancing age can adversely affect a thoroughbred brood-mare’s reproductive efficiency and influence the commercial and athletic potential of her progeny. Causes for the decline in fertility include decreased oocyte and embryo quality, anatomical defects and endometrial degeneration. In addition, evidence exists that as the age of a dam increases, her foals will be at increased risk of morbidity and mortality during the neonatal period. Health issues can have lasting and deleterious effects on surviving foals, including decreased sale value and reduced athletic performance. The purpose of this review is to evaluate the association between mare age, fertility and offspring vigour in thoroughbred horses. Additional keywords: maternal age, offspring health, subfertility. Received 13 October 2014, accepted 17 February 2015, published online 19 March 2015
Introduction Contrary to a contemporary aphorism, age is, indeed, more than a number as it pertains to reproductive efficiency and offspring vitality in thoroughbred horses. The correlation between advancing age and declining fertility is a phenomenon fairly ubiquitous among domestic animals. In food animals, this corollary leads to regular culling of older animals and replacement with younger animals. Doing so is done for both economic and management reasons, such as improving herd fertility rates, increasing genetic diversity or exploiting a certain phenotype. Horses offer a unique contrast to other livestock when it comes to selection of breeding stock. First, the primary function of horses is that of athletic performance and recreation, not food or fibre production; thus, less emphasis is placed on fertility when selecting breeding stock. Second, the commercial value of individual horses often far exceeds that of other farm animals and money spent towards obtaining a single live foal can extend into the tens, if not hundreds, of thousands of dollars when factoring in stud fees and labour. A third distinction is that owners place a significant amount of sentimental value on their horses. There is a large contingent of equestrians who consider their horses to be pets, or even immediate members of their families, and not farm animals. Fourth, the gestation length of horses is longer than most other domestic animals. When coupled with an extended gap from birth to the onset of training (,2 years), several years, and hence several foal crops, are needed to determine the worthiness of a sire or dam as producers of quality offspring. As it relates specifically to North American thoroughbreds, breeding and registration requires strict adherence to the rules and regulations set forth by The Jockey Club (http://www.registry. jockeyclub.com/registry.cfm?Page=tjcRuleBook, accessed 3 Journal compilation Ó CSIRO 2015
March 2015). The one notable and rather unique (compared with other breed registries) requirement for registration is that all thoroughbreds must be conceived via the act of live cover. This rule precludes the use of any assisted reproductive technique (ART), whether it is artificial insemination, embryo transfer or other in vitro methods of fertilisation, such as intracytoplasmic sperm injection. The consequences of this rule are numerous and far-reaching, particularly as it relates to reproductive management of thoroughbred brood-mares. Not only must mares conceive and carry a foal to term, but they must also do so with regularity to remain profitable. What is more, most commercial thoroughbred breeders will continue to breed aged animals well beyond their reproductive prime, especially those that are proven producers of quality blood stock. Interestingly, and contrary to this notion, there are several scientific studies that suggest younger mares are more likely to produce quality offspring as opposed to their older counterparts (Finocchio 1985; Lema and Finocchio 1985; Barron 1995; Morley and Townsend 1997). Economic analyses and certain observational studies offer intriguing viewpoints regarding the commercial value and productivity, in terms of both economic and athletic performance, of offspring of older mares. Certain accounts demonstrate that even the most blue-blooded of mares will only produce one high-quality individual in her lifetime (Finocchio 1985), whereas others point out notable exceptions to this observation, thereby spurring the desire to breed older mares in an attempt to catch lighting in a bottle one more time (Consignors 2007). As discussed below, there is a significant association between mare age and various reproductive measures. The consequences of aging are multifactorial and often cumulative, whereas the fallouts of breeding older mares have both direct www.publish.csiro.au/journals/rfd
Effect of age on fertility in thouroughbred mares
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Table 1. Measures of reproductive performance in brood-mares, adapted from Nath (2011) and Ginther (1993) Pregnancy rate per cycle First cycle pregnancy rate Seasonal pregnancy rate Live-foal rate Embryonic loss rate Fetal loss rate Abortion rate Services per pregnancy Cycles per pregnancy
Percentage of mated mares that are pregnant on a specified day after mating Percentage of mares that are pregnant after the first mated oestrus Percentage of mares that are pregnant at the end of the breeding season Percentage of mated mares that produce a live foal Percentage of fertilised oocytes that do not survive to 42 days after mating Percentage of pregnancies surviving to 42 days that do not result in a live foal General term regarding pregnancy loss that needs to be defined in relation to stage of gestation Number of times a mare is served before diagnosis of pregnancy Number of served oestrous cycles before the mare becomes pregnant in one season
and indirect effects on them and their offspring. Most notably, these effects can influence the commercial value of the mare, as well as the future value of a foal as either a commodity or athlete. How old is too old? Before attempting to answer this question, it is important first to define certain parameters used to quantify reproductive efficiency in brood-mares. As adapted from Ginther (1993) and recently described by Nath (2011), commonly used measures are listed in Table 1. Hereto forth, when describing the day of pregnancy and gestation, that day will be in reference to the day of the last mating, which is defined as Day 0. Not surprisingly, there is no hard and fast rule for the age at which mares will experience a decline in fertility. This age varies among individuals, farms and locales. Nevertheless, a review of the literature clearly demonstrates that age is one of the most consistent factors dictating a mare’s reproductive capacity. An early report from the US indicated that seasonal pregnancy rates started to decline gradually in mares aged 13 years and older (Hutton and Meacham 1968). More recent reports from central Kentucky, USA (Baker et al. 1993; Bosh et al. 2009a), Newmarket, UK (Morris and Allen 2002; Allen et al. 2007), and Victoria, Australia (Bru¨ck et al. 1993; Nath 2010), scrutinised this phenomenon further by evaluating several different reproductive parameters from data collected from regional stud farms. As indicated in Table 2, when mares were divided into certain age groups, early (Day 15–21) per cycle pregnancy rates began to wane, on average, when mares reached 14 years of age. Day 40–42 per cycle pregnancy rates for the US and UK appeared to decline at an even earlier age (Table 3), and data from both countries demonstrate a progressive drop with advancing age groups. With respect to embryonic death rates (defined as early detection of a pregnancy followed by loss at or before 42 days gestation), equivocal results were reported among the different studies in that the ages at which a significant interaction occurred varied between different regions (Table 4). Regardless, the incidence escalated with increasing age, with the youngest group of mares having the lowest frequency of embryonic death. It was intriguing to observe that the study from Australia (Nath 2010) reported an embryonic loss rate of 11.8% in mares aged .18 years. This value appears to be substantially lower than values from studies out of central Kentucky (23.1%; Bosh et al. 2009a) and Newmarket (18.6%; Allen et al. 2007). The
Table 2. Early (approximately Days 15–21) per cycle pregnancy rates for thoroughbred brood-mares grouped by age in various regions of the world Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) Age (years) 2–8 9–13 14–18 .18
USA
UKB
AustraliaC
66.3%a 65.6%a 61.0%ab 48.1%b
67.3%a 63.4%a 58.3%b 54.9%b
72.1%a 69.8%a 61.7%b 55.0%b
A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007). C Adapted from Nath (2010). B
Table 3. Day 40–42 per cycle pregnancy rates for thoroughbred brood-mares grouped by age in the US and UK Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) USA
UKB
63.2%a 59.0%a,b 50.8%bc 37.0%c
63.0%a 58.5%b 52.0%c 43.8%d
Age (years) 2–8 9–13 14–18 .18 A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007).
B
Table 4. Embryonic death rates for thoroughbred brood-mares grouped by age in various regions of the world Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) Age (years) 2–8 9–13 14–18 .18 A
USA
UKB
AustraliaC
4.6%a 10.1%a,b 16.7%b 23.1%b
5.9%a 7.1%a 10.0%b 18.6%c
5.1%a 7.9%b 10.0%b 11.8%b
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007). C Adapted from Nath (2010). B
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Table 5. Seasonal Day 40–42 pregnancy and live-foal rates in thoroughbred brood-mares grouped by age in the US and UK Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) USA
Age (years) Day 40 (%) 2–8 9–13 14–18 .18
a
93.7 90.2a 80.9b 67.2b
UKB
Live-foal (%) a
82.9 80.1a 68.4b 55.2b
Day 42 (%) a
91.2 87.9b 83.5c 73.6d
Live-foal (%) 81.8a 76.8b 73.1b 62.8c
A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007).
B
reasons for this perceived discrepancy are not immediately known, but may be due to differences in reproductive management, mare status and stallion fertility. Moreover, fetal loss and live foal rates were not reported in the study of Nath (2010) as they were in the other studies, which, if available, would help better elucidate the disparity in results. Age also significantly impacts seasonal pregnancy and livefoal rates (Table 5). In central Kentucky, both these measures were similar between mares aged 2–8 and 9–13 years of age, but decreased significantly in the two older age groups (14–18 years and .18 years). In Newmarket, Day 42 pregnancy rates decreased with each successive age group. In addition, the youngest group of mares had higher live-foal rates than the other groups. Predictably, mares aged .18 years had significantly lower live-foal rates compared with the other age groups. Differences in these results could be related to difference in sample sizes between the two studies. Bosh et al. (2009a) tallied records from a total of 1011 mares over 1559 oestrous cycles, whereas Allen et al. (2007) had over threefold as many mares and cycles, which likely improved statistical power and reduced the likelihood of Type II errors. In contrast with the previously discussed studies, a report out of Sweden (Hemberg et al. 2004) found that mare age did not have a significant effect on per cycle pregnancy rates. However, these researchers used different age groupings, with the oldest group comprising mares .13 years of age. Furthermore, they did find a significant association between increasing age and increasing pregnancy loss and decreasing live-foal rates, findings that are in agreement with other studies from central Kentucky (Baker et al. 1993; Bosh et al. 2009a), Newmarket (Morris and Allen 2002; Allen et al. 2007) and Victoria (Bru¨ck et al. 1993; Nath 2010). A final observation pertains to the relative intensity of management as the age of a mare increases. For example, Allen et al. (2007) reported that mares 9 years of age or older required more covers to obtain a Day 15 pregnancy than younger mares. They also demonstrated a significant increase between groups in the percentage of mares given uterine treatments. The implications of these findings are that older mares require more intensive veterinary management, which translates into more time, resources and money needed to obtain a pregnancy. The aforementioned studies provide strong evidence that as the age of a thoroughbred mare increases, her reproductive
efficiency decreases. This decrease is manifested in declining pregnancy rates (both per cycle and seasonal) and live-foal rates, as well as increased embryonic and fetal loss rates. In addition, there is some evidence supporting the notion that the incidence of embryonic loss appears to increase sooner, with respect to age, than per cycle and seasonal pregnancy rates in mares. This finding could influence future management strategies in that certain proactive measures (e.g. more aggressive pre- and postbreeding management, routine and serial pregnancy examinations, progesterone supplementation and vulvoplasties) could be taken to reduce the risk of embryonic and fetal loss in relatively young mares. However, and as mentioned previously, increasing the intensity of management can lead to increasing expenses to produce a pregnancy and generate a live foal. Age-related factors affecting reproductive efficiency The causes for the association between increasing mare age and the decline in fertility are numerous and multifactorial. Examples include reduced oocyte and embryonic viability, degenerative changes to the external and internal reproductive tract and changes in the development of fetal membranes. These factors are not mutually exclusive and can occur in tandem to cause reductions in the various measures of reproductive efficiency discussed above. Scientific studies have provided sound evidence of the association between declining oocyte viability and advancing mare age. Using oocyte transfer (OT), Carnevale and Ginther (1995) showed that oocytes from older donor mares resulted in significantly fewer pregnancies than those from younger donor mares when oocytes were transferred into young recipient mares. Advancing age has also been postulated as being the primary determinant for the relative success (or lack thereof) of obtaining pregnancies from older mares in a commercial OT program (Carnevale et al. 2001). Reduced oocyte quality, and hence decreased pregnancy rates, in older mares may be due to age-related morphological differences in oocytes. Increased vacuolisation of and changes in the shape of oocytes were more commonly seen in older compared with younger mares when both light and electron microscopy were used to evaluate oocytes from mares of different ages (Carnevale et al. 1999). Using a clinical grading system based on cumulus cell expansion and the appearance of the ooplasm, oocytes from mares $20 years of age had poorer morphological grades compared with younger mares (Carnevale et al. 2005). More recently, Rambags et al. (2006, 2014) demonstrated a reduced quantity of mitochondria in in vitro-matured oocytes from older compared with younger mares. They also used transmission electron microscopy to reveal morphological changes in mitochondria from oocytes of older mares, such as swelling and loss of internal architecture. These studies have immediate practical considerations. Changes seen in oocytes of older mares could alter the complex and highly energy-dependent events involved in oocyte maturation, thereby leading to a reduction in oocyte viability. As a result, embryo developmental rates could be negatively affected, ultimately resulting in reduced pregnancy rates and/or increased embryonic loss more commonly seen in aged mares (Ball et al. 1989; Ball 2011). Embryo transfer of Day 4 embryos
Effect of age on fertility in thouroughbred mares
collected from old, subfertile donors into normal recipients yielded significantly lower Day 14 pregnancy rates compared with transfer of embryos from young, normal donors (Ball et al. 1989). In addition, Carnevale et al. (1993) reported smaller embryonic vesicle sizes and lower Day 11 pregnancy rates in old mares relative to young mares. Differences in morphological embryonic development rates between young and old mare donors has also been documented, with embryos collected from older donors and cultured in vitro having more microscopic abnormalities than those from younger mares (Brinsko et al. 1994). Changes in the quality and character of the embryo may be a result of aneuploidy, which could account for a significant portion of early embryonic loss in brood-mares. Previous work by Ball et al. (1989) showed that despite relatively high early (Day 4) pregnancy rates, embryonic development was either delayed or lower in embryos transferred from older mares during subsequent pregnancy examinations. Derangements in chromosomal structure and DNA replication can alter proper development of human embryos, and the rate of aneuploidy has been shown to increase with increasing age in women (Nagaoka et al. 2012). This phenomenon has not been thoroughly investigated in the horse, but it likely represents a realistic means for the increased frequency of embryonic loss seen in older mares. Anatomically, one of the most well-documented changes in thoroughbred brood-mares is worsening of perineal conformation with age. First described by Caslick (1937), poor vulvar conformation was most commonly seen in older multiparous mares and was shown to adversely affect reproductive performance. The effect on fertility is related to aspiration of air and faecal contents into the vagina, which causes inflammation and colonisation of bacteria in the reproductive tract, including the uterus. The most common clinical presentation is a decreased angle of declination of the vulva with respect to the horizontal plane, a shortened vulva and a sunken anus. Treatment typically entails performing a Caslick vulvoplasty (also known as ‘Caslick’, ‘vulvoplasty’ or ‘suture’). The need for this surgery can be determined by calculating the Caslick index as described by Pascoe (1979); however, most practitioners will forgo the calculation and instead perform the procedure in mares with a history of subfertility. Agreement generally exists among theriogenologists that once a mare has a vulvoplasty, she will require one during successive pregnancies (Bradecamp 2011). In thoroughbred foaling mares, a vulvoplasty is usually performed within a week after foaling. The benefits include reducing the severity of endometritis, as well as improving first cycle pregnancy rates and live-foal rates. A study evaluating vulvar conformation and its relationship to endometrial cytology and fertility in thoroughbred mares underscored the importance of maintaining a vulvoplasty during subsequent pregnancies (Hemberg et al. 2005). Mares that were not re-sutured after parturition had a significantly higher incidence and increased severity of endometritis compared with mares that were sutured shortly after foaling. The former group also had significantly lower first-cycle pregnancy and live-foal rates compared with the latter group, further emphasising the importance of performing a vulvoplasty in a timely manner after foaling.
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No matter how well managed a mare is, she will, with advancing age, develop progressive changes to her endometrium (Rickets and Alonso 1991). These changes are associated with lower live-foal rates (Kenney 1978). Inflammatory cell infiltrates, glandular fibrosis and nesting and lymphangiectasia are common histopathological findings that, when combined with a history of subfertility, comprise the disease complex known as chronic degenerative endometritis (CDE; Allen 1993). Because the relative intimacy of the fetal–maternal interface is extremely influential with respect to nutrient exchange and promoting proper development of the fetus, a possible consequence of CDE is reduced development and efficiency of the fetal membranes. Using light and scanning electron and transmission electron microscopy, Bracher et al. (1996) examined the ultrastructural attachments of the endometrium and allantochorion in normal pregnant mares and pregnant mares with CDE. They were able to discern a delay in and reduction of microcotyledon development in mares with CDE compared with normal mares. More recently, this same laboratory used stereology to examine the impact of age and parity on fetal membrane development for term pregnancies (Wilsher and Allen 2003). Their results demonstrated that the surface density of the microcotyledons was significantly lower in multiparous mares 16 years of age or older compared with younger primaparous and multiparous mares. Thus, there is a possibility that differences in the development of equine fetal membranes seen in older mares could increase the risk of fetal growth retardation and/or fetal demise. This notion also corresponds with the longheld belief among some thoroughbred breeders that mares tend to have skinnier and poorer looking foals later in life, hence spawning the colloquial term ‘old mare foal’. However, the scientific evidence suggests otherwise, because neither the efficiency of fetal membranes nor foal birthweights were significantly reduced in older compared with younger mares (Wilsher and Allen 2003). These results were confirmed in a more recent report and parity was instead shown to be the primary factor influencing foal birthweight in that for every extra foaling, birthweight increased by 0.8 kg (Elliott et al. 2009). Despite these conflicting results, it would be a mistake to discount the effect of mare age on fetal development, the reason being the intimate link between age and parity. Not only do most thoroughbred brood-mares start their reproductive careers at a relatively young age (3–6 years of age), but they must also carry their pregnancies to term. Thus, age and parity are almost inseparable and enjoy a synergistic relationship with respect to reproductive efficiency in thoroughbred mares. The author is aware of the potential for confounding results when the two are not separated (Elliott et al. 2009), but will not henceforward quibble over the distinction. Advancing mare age and its influence on offspring vigour and value One of the primary objectives of thoroughbred breeders is to raise horses in a manner that allows them to realise their full athletic potential. Thoroughbred breeding is also big business
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and the money involved at public auctions generates added pressure on breeders and consignors to present a commercially appealing product. Producing a quality athlete and/or marketable prospect involves a confluence of factors, with mare age being a polemical element involved in achieving success in the thoroughbred industry. As discussed below, advancing mare age not only has measurable effects on foal health, performance and profit, but it can also introduce bias against the relative commercial value of both a dam and her offspring. The first year of life is one of the more formative times of a horse’s life. Mitigation and management of disease are essential during this phase, because disease can have lasting and potentially disastrous consequences on athletic performance. For example, bacteraemic neonatal foals have been shown to have fewer wins and total earnings than maternal siblings (Sanchez et al. 2008). Morley and Townsend (1997) demonstrated the negative impact of foal illness on commonly sought-after physical attributes for racing performance. Sick neonates (#14 days of age) were fivefold more likely to be considered unsuitable as equine athletes assuming they reached 1 year of age, whereas foals between the ages of 15 days and 1 year experiencing health issues were sevenfold more likely to be deemed unacceptable for athletic performance at 1 year of age. Morley and Townsend (1997) also identified increasing mare age as a major risk factor for morbidity and mortality in both neonates and foals between the ages of 15 days and 1 year. The average age for dams of foals experiencing health issues (11.4 years) or dying during the neonatal period (12.4 years) was significantly higher than for dams of foals not experiencing health problems (10.6 years) or surviving to 15 days of life (10.6 years). In addition, the mean age of mares with foals that died between 15 days and 1 year (13.1 years) was higher than that of mares with foals that survived past 1 year of age (10.6 years). Angular limb deformities (ALD) were cited as the specific health issue that had the highest likelihood of producing an unsatisfactory physical assessment. Causation for the association between mare age and increased risk of foal morbidity and mortality were not immediately evident from that study. Morley and Townsend (1997) did speculate that there may be a link between endometrial degeneration and foal illness. Altered nutrient exchange and energy partitioning could adversely affect fetal development and certain parturient events (e.g. colostrum production and milk let-down) required for neonatal growth and development. Adverse health events early in life can also impact future athletic ability. For racehorses, speed ratings are commonly used measures to express the racing merit of an individual horse. In the UK, Timeform ratings are an example of such a metric. The higher the rating, the better the performance, with superior horses rating at or above 130 and inferior horses in the 50s or lower. To evaluate the effect of mare age and parity on progeny Timeform ratings, a small (n ¼ 81) study was conducted that selected for mares that had at least eight live foals, two of which had obtained a Timeform rating of $110 (Barron 1995). Ratings for offspring peaked at a maternal age of 9 years and declined significantly thereafter. A similar effect of parity on Timeform ratings was seen (i.e. as parity increased, ratings decreased). A more recent and larger (n ¼ 431) study provided somewhat
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opposing results (Wilsher et al. 2006). No significant effect of mare age or parity was observed with respect to the likelihood of progeny running as 2 or 3 year olds, winning a race or performance based on Timeform ratings. However, as Wilsher et al. (2006) point out, their study only considered one offspring per dam, so the differences in study design and sample selection between the two papers may account for the divergent results. Nonetheless, the disparity in outcomes between studies introduces the element of class, another measure of potential and performance, and its relationship with age. ‘Class’ is a term used to describe both tangible and intangible virtues of racehorses that, collectively, serve as an indicator for their relative skill level. Quantitative measures of class are calculated similar to speed ratings and are based primarily on past performances, such as timed work-outs and races. More esoteric indicators of class are pedigree, physical stature, tactical speed, grit and heart. Thus, ‘class’ is a fluid and somewhat amorphous concept that can change throughout an individual racehorse’s career. One of the capstones of class is winning a stakes race. When investigating the progeny performance of 1641 brood-mares who produced 18 931 foals, an astounding 11.5 foals per mare, Finocchio (1985) reported that 14.5% of these foals became stakes winners. Also of note was the fact that 43.3% of these mares produced more than one stakes winner. When factoring in age and parity, stakes-producing ability declined in a nearly linear fashion after 7 years of age and the likelihood of producing a stakes winner waned progressively beginning with the sixth parity. Statistical analyses of these data revealed that mares #10 years of age produced a greater proportion of stakes winners than those aged .10 years. When evaluating birth ranks (i.e. the order in which a foal was born from an individual mare), a larger proportion of foals with birth-ranks ,6 were stakes winners compared with foals with higher birth-ranks (Lema and Finocchio 1985). When taken as a whole, these results provide testimony to the perception within the thoroughbred breeding business that class begets class. Unfortunately, and as most breeders and owners would attest to, there is no ‘sure thing’ when it comes to breeding for performance and profit. The element of uncertainty looms large in thoroughbred breeding, thereby making it a stochastic or unpredictable process. The inexact nature of equine reproduction has been shown to have direct consequences on economic returns and profitability. As demonstrated by Bosh et al. (2009b), brood-mares are long-term investments with positive gains dependent on their reproductive efficiency over the course of several years. Profits and rates of return were greatest for maiden mares that produced a registered foal for seven consecutive years before being sold or those that were bred for 9 years and only barren one time 4 years into their production history. Not surprisingly, these researchers identified increasing mare age as a significant factor that limited the odds of producing a registered foal and, summarily, a positive financial yield. Thus, mares should start their reproductive careers early and remain consistently productive. Doing so optimises the likelihood of producing a viable foal and reaping a positive investment. Economic analyses of yearling thoroughbred public auctions illustrate the importance of mares maintaining satisfactory reproductive efficiency and producing quality offspring. In an
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early study by Commer (1990), the month of birth was shown to influence the amount buyers were willing to spend on yearlings. Those that foaled in January and February of the previous year were estimated to sell for almost US$2000 more than yearlings born in May or June. The preference of buyers for older yearlings was confirmed and expanded a few years later, in which yearlings born in January–March fetched significantly higher prices than those born in later months (Buzby and Jessup 1994). When the age of the yearlings was measured in days between foaling and the first day of the auction, Chezum and Wimmer (1997) described a significant association between increasing yearling age and sale price. Finally, when examining quantifiable determinants of auction prices in thoroughbred yearlings over a 13-year period, researchers calculated that yearlings born after April were worth 30% and 18% less than those born in January–February and March–April, respectively (Robbins and Kennedy 2001). The measurable preference for older yearlings is likely due to their physical maturity. Precocity is a highly sought after trait that can translate into successful racing performance as 2 or 3 year olds. Therefore, it behoves commercial breeders to have mares foal early and often to generate precocious offspring, which helps maximise revenue. The Keeneland November Breeding Stock Sale, Lexington, Kentucky, USA is the largest thoroughbred sale of its kind in the world. Econometric studies have been useful when evaluating factors influencing the thoroughbred brood-mare market. Analyses of the summary statistics from past sales identified reproductive efficiency and age as major elements influencing the commercial value of all brood-mares sold. For the 1996 sale, Neibergs (2001) calculated that barren mares had a marginal value discount of US$15 010 stemming from increased production costs in maintaining an open mare and increased risk of poor reproductive soundness. Based on an average age of 9 years, Neibergs (2001) also found that brood-mares lose US$3051 in value for each additional year of age relative to the mean. When studying hammer prices from the 2005 sale, Maynard and Stoeppel (2007) chose to exclude barren mares from their analysis. Removing this particular group was thought to eliminate inherent differences between these two groups of mares, which could have potentially confounded results in the study of Neibergs (2001). Consequently, Maynard and Stoeppel (2007) determined that each additional year of a brood-mare’s age dropped her value by nearly US$12 000. Inflation no doubt played a role in the relative discounts of price attributed to age between these studies, yet there is no ignoring the importance of age when determining the relative commercial value of a broodmare. The age of the mare reflects her potential future earnings from foal production. The younger the mare, the more foals she is capable of producing, thereby increasing her chances of being a successful producer. Ageism: perception versus reality On the surface, culling older mares and selecting offspring from young, healthy mares seems like a practical and financially sound method to breed, raise and race thoroughbreds. Because age is one of the few variables that can actually be controlled for, using this parameter to decide when and which mare to cull
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could be seen as a shrewd method of management. Ageism, some thoroughbred industry analysts would argue, can effectively strengthen the odds of obtaining a top class equine athlete. In his landmark report, Dink (1990) reported that of 137 184 foals to race, 4804 (3.50% overall) were stakes winners and the highest percentage of stakes winners were out of mares that were 4–10 years of age (3.87%). The percentage gravitated mostly downwards from there; mares aged 11–15 years produced 3.32% stakes winners, whereas those aged 16–20 years produced 2.33% stakes winners. Both Rogers (2014) and Tapp (2014) evaluated summary statistics from the 2002–11 Keeneland September Yearling Sales to calculate the average class performance index (CPI) of graduates from this sale. The CPI is used to rank runners by their average earnings per start compared with age- and sex-matched peers. There was a steady downward trend in CPI after a mare’s third foal (Tapp 2014). Another interesting tendency was observed when foal count was charted as a function of average sale price and CPI. As described by Rogers (2014), the average sale price of a mare’s first six foals roughly followed a similar path of the average CPI for these foals. By the seventh foal, there was a precipitous drop in average CPI. Conversely, the average sale price actually increased with the seventh foal. This phenomenon was possibly related to buyers paying a premium for either yearlings out of proven mares or residual bloodstock value of a filly. Nevertheless, if the goal was to purchase a solid racing prospect, paying this premium effectually placed the buyers at a disadvantage when attempting to recoup costs of the purchase due to the likelihood of paying more for a lesser product based on these analytics. As mentioned previously, culling and selection based on age seem commonsensical, especially considering the favourable results obtained when using such a criterion in other livestock species. But, when comparing and contrasting different factors, it is not without its problems. The low cull value of a mare coupled with the high cost of a replacement makes such a practice in mares less economically viable than in other species (Bosh et al. 2009b). Selection based on age also does not translate into guaranteed success on the racetrack, for there are plenty of examples of top class racehorses produced out of older mares. From 1984 to 2006, there were 15 Breeder’s Cup Champions that were out of mares older than 16 years of age (Consignors and Commercial Breeders Association 2007). Then, there is the individual example of the prolific Somethingroyal who was 18 years old when she foaled the immortal and unequalled Secretariat and produced two more stakesplaced horses at 19 and 20 years of age. Somethingroyal is obviously an exception to the rule that age adversely affects fertility and offspring vigour, but she is an unmistakable exception nonetheless. Her produce record serves as a reminder that mares can age and produce at different rates due to a conflux of both genetic and environmental factors, thereby giving breeders pause when contemplating culling an older mare from a breeding program. In addition, it would be contemptuous of us clinicians to ignore the emotional value of brood-mares. Some of these mares may represent an owner’s first winner or a family’s breeding legacy, which contributes added yet immeasurable value to the mare above and beyond her market price.
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Finally, ageism in thoroughbreds may represent a sublime Darwinian concept or a surreptitious method to improve the breed. The requirement that all foals must be conceived via the act of live-cover and carried to term by their dam selects for fertility to a much greater extent than what is seen in other breeds that allow the use of ART. Further, if an aged mare has maxed out her potential as a quality producer, her offspring will be a reflection of such, effectively removing her from both the commercial market and the breeding population. Thus, it seems that ageism is both perception and reality, which represents a microcosm of the racing industry itself. Attempting to establish a set formula guaranteeing success is impossible, if not unrealistic, to attain due to a legion of prominent and, at times, paradoxical factors. However, thoroughbred breeding can be lucrative, with the economic impact in central Kentucky alone estimated to be in the billions of dollars (Kentucky Horse Council 2013). When combined with the allure and lustre of owning and racing elite equine athletes, the motivation will likely always exist to search for a sweeping edict securing prosperity in this industry. Conclusions As judged by pregnancy, embryonic loss and live-foal rates, advancing mare age can adversely affect reproductive efficiency. Neonatal vigour also appears to be dependent on the age of the dam in that foals from older mares appear more prone to morbidity and mortality than those out of younger mares. Evidence exists for an association between athletic performance of the progeny and mare age, but this relationship likely works in synergy with parity. Similarly, the commercial value of either a mare or her produce can be affected by age and parity, although buyers are willing to pay a premium for offspring from older mares despite increased risks of diminished returns on their investment. Mare age has a complicated and perplexing relationship within the thoroughbred industry. As researchers and clinicians, we should continue to explore this relationship to help evolve the industry and sustain the welfare of its most precious commodity, the horse. References Allen, W. R. (1993). Proceedings of the John P. Hughes International Workshop on Equine Endometritis. Equine Vet. J. 25, 184–193. Allen, W. R., Brown, L., Wright, M., and Wilsher, S. (2007). Reproductive efficiency of Flatrace and National Hunt thoroughbred mares and stallions in England. Equine Vet. J. 39, 438–445. doi:10.2746/ 042516407X1737581 Baker, C. B., Little, T. V., and McDowell, K. J. (1993). The live foaling rate per cycle in mares. Equine Vet. J. Suppl. 25(S15), 28–30. Ball, B. A. (2011). Embryonic loss. In ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2327–2336. (Wiley-Blackwell: Ames, IA.) Ball, B. A., Little, T. V., Weber, J. A., and Woods, G. L. (1989). Survival of Day 4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J. Reprod. Fertil. 85, 187–194. doi:10.1530/JRF.0.0850187 Barron, J. K. (1995). The effect of maternal age and parity on the racing performance of thoroughbred horses. Equine Vet. J. 27, 73–75. doi:10.1111/J.2042-3306.1995.TB03036.X
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Bosh, K. A., Powell, D., Shelton, B., and Zent, W. (2009a). Reproductive performance measures among thoroughbred mares in central Kentucky, during the 2004 mating season. Equine Vet. J. 41, 883–888. doi:10.2746/ 042516409X456068 Bosh, K. A., Powell, D., Neibergs, J. S., Shelton, B., and Zent, W. (2009b). Impact of reproductive efficiency over time and mare financial value on economic returns among thoroughbred mares in central Kentucky. Equine Vet. J. 41, 889–894. doi:10.2746/042516409X456059 Bracher, V., Mathias, S., and Allen, W. R. (1996). Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Equine Vet. J. 28, 180–188. doi:10.1111/J.2042-3306.1996. TB03771.X Bradecamp, E. A. (2011). Pneumovagina. In ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2537–2544. (Wiley-Blackwell: Ames, IA.) Brinsko, S. P., Ball, B. A., Miller, P. G., Thomas, P. G. A., and Ellington, J. E. (1994). In vitro development of Day 2 embryos obtained from young, fertile mares and aged, subfertile mares. J. Reprod. Fertil. 102, 371–378. doi:10.1530/JRF.0.1020371 Bru¨ck, I., Anderson, G. A., and Hyland, J. H. (1993). Reproductive performance of thoroughbred mares on six commercial stud farms. Aust. Vet. J. 70, 299–303. doi:10.1111/J.1751-0813.1993.TB07979.X Buzby, J. C., and Jessup, E. L. (1994). The relative impact of macroeconomic and yearling-specific variables in determining thoroughbred yearling price. Appl. Econ. 26, 1–8. doi:10.1080/00036849400000055 Carnevale, E. M., and Ginther, O. J. (1995). Defective oocytes as a cause of subfertility in old mares. Biol. Reprod. Mono. 1, 209–214. Carnevale, E. M., Griffin, P. G., and Ginther, O. J. (1993). Age-associated subfertility before entry of embryos into the uterus of mares. Equine Vet. J. 25, 31–35. doi:10.1111/J.2042-3306.1993.TB04820.X Carnevale, E. M., Uson, M., Bozzola, J. J., King, S. S., Schmitt, S. J., and Gates, H. D. (1999). Comparison of oocytes from young and old mares with light and electron microscopy. Theriogenology 51, 299. doi:10.1016/S0093-691X(99)91858-7 Carnevale, E. M., Squires, E. L., Maclellan, L. J., Alvarenga, M. A., and Scott, T. J. (2001). Use of oocyte transfer in a commercial breeding program for mares with reproductive abnormalities. J. Am. Vet. Med. Assoc. 218, 87–91. doi:10.2460/JAVMA.2001.218.87 Carnevale, E. M., Coutinho da Silva, M. A., Panzani, D., Stokes, J. E., and Squies, E. L. (2005). Factors affecting the success of oocyte transfer in a clinical program for subfertile mares. Theriogenology 64, 519–527. doi:10.1016/J.THERIOGENOLOGY.2005.05.008 Caslick, E. A. (1937). The vulva and the vulvo–vaginal orifice and its relation to genital health of the thoroughbred mare. Cornell Vet. 27, 178–187. Chezum, B., and Wimmer, B. (1997). Roses or lemons: adverse selection in the market for thoroughbred yearlings. Rev. Econ. Stat. 79, 521–526. doi:10.1162/REST.1997.79.3.521 Commer, M. (1990). The effect of non-phenotypic data on thoroughbred prices in the mid-Atlantic market. Prof. Anim. Sci. 7, 18–24. Consignors and Commercial Breeders Association (2007). Myth #3: foals out of older mares. In: ‘Buying Sales Yearlings: Plain and Simple’. (Eds R. Manseau.) pp. 24–25. (The Conignors and Commercial Breeders Association: Lexington, KY.) Kentucky Horse Council (2013). ‘2012 Kentucky Equine Survey.’ (University of Kentucky Ag Equine Programs: Lexington, KY.) Dink, D. (1990). Advantages of a February foal. Thoroughbred Times May 4, 28–32. Elliott, C., Morton, J., and Chopin, J. (2009). Factors affecting foal birth weight in thoroughbred horses. Theriogenology 71, 683–689. doi:10.1016/J.THERIOGENOLOGY.2008.09.041 Finocchio, E. J. (1985). Race performance and its relationship to birthrank and maternal age – I. In: ‘Proceedings From the 31st Annual Convention
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of the American Association of Equine Practitioners’. pp. 571–577. (AAEP: Lexington, KY.) Ginther, O. J. (1993). Reproductive efficiency. In ‘Reproductive Biology of the Mare: Basic and Applied Aspects’, 2nd edn. (Ed. O. J. Ginther.) pp. 499–562. (Equiservices Publishing: Cross Plains, WI.) Hemberg, E., Lundeheim, N., and Einarsson, S. (2004). Reproductive performance of thoroughbred mares in Sweden. Reprod. Domest. Anim. 39, 81–85. doi:10.1111/J.1439-0531.2004.00482.X Hemberg, E., Lundeheim, N., and Einarsson, S. (2005). Retrospective study on vulvar conformation in relation to endometrial cytology and fertility in thoroughbred mares. J. Vet. Med. A Physiol. Pathol. Clin. Med. 52, 474–477. doi:10.1111/J.1439-0442.2005.00760.X Hutton, C. A., and Meacham, T. N. (1968). Reproductive efficiency on Fourteen Horse Farm. J. Anim. Sci. 27, 434–438. Kenney, R. M. (1978). Cyclic and pathologic changes of the mare endometrium as detected by biopsy, with a note on early embryonic death. J. Am. Vet. Med. Assoc. 172, 241–262. Lema, J.-A. S., and Finocchio, E. J. (1985). Race performance and its relationship to birthrank and maternal age – II. In: ‘Proceedings From the 31st Annual Convention of the American Association of Equine Practitioners’. pp. 577–578. (AAEP: Lexington, KY.) Maynard, L. J., and Stoeppel, K. M. (2007). Hedonic price analysis of thoroughbred broodmares in foal. J. Agribusiness 25, 181–195. Morley, P. S., and Townsend, G. G. (1997). A survey of reproductive performance in thoroughbred mares and morbidity, mortality and athletic potential of their foals. Equine Vet. J. 29, 290–297. doi:10.1111/J.2042-3306.1997.TB03126.X Morris, L. H. A., and Allen, W. R. (2002). Reproductive efficiency of intensively managed thoroughbred mares in Newmarket. Equine Vet. J. 34, 51–60. doi:10.2746/042516402776181222 Nagaoka, S. I., Hassold, T. J., and Hunt, P. A. (2012). Human aneuploidy: mechanism and new insights into an age-old problem. Nat. Rev. Genet. 13, 493–504. doi:10.1038/NRG3245 Nath, L. C. (2010). Reproductive efficiency of thoroughbred and standardbred horses in north-east Victoria. Aust. Vet. J. 88, 169–175. doi:10.1111/J.1751-0813.2010.00565.X
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Nath, L. C. (2011). Reproductive efficiency. In: ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2779–2789. (Wiley-Blackwell: Ames, IA.) Neibergs, J. S. (2001). A hedonic price analysis of thoroughbred broodmare characteristics. Agribusiness 17, 299–314. doi:10.1002/AGR.1017 Pascoe, R. R. (1979). Observations on the length and the angle of declination of the vulva and its relation to fertility in the mare. J. Reprod. Fertil. Suppl. 27, 299–305. Rambags, B. P. B., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2006). Oocyte mitochondrial degeneration during reproductive ageing in the mare. Havemeyer Found. Monogr. Ser. 18, 25–27. Rambags, B. P., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2014). Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81, 959–965. doi:10.1016/ J.THERIOGENOLOGY.2014.01.020 Ricketts, S. W., and Alonso, S. (1991). The effect of age and parity on the development of chronic endometrial disease. Equine Vet. J. 23, 189–192. doi:10.1111/J.2042-3306.1991.TB02752.X Robbins, M., and Kennedy, P. E. (2001). Buyer behavior in a regional thoroughbred yearling market. Appl. Econ. 33, 969–977. doi:10.1080/ 00036840010002529 Rogers, B. (2014). Ageism at yearling sales. Bluebloods September, 37. Sanchez, L. C., Giguere, S., and Lester, G. D. (2008). Factors associated with survival of neonatal foals with bacteremia and racing performance of surviving thoroughbreds: 423 cases (1982–2007). J. Am. Vet. Med. Assoc. 233, 1446–1452. doi:10.2460/JAVMA.233.9.1446 Tapp, I. (2014). Young mares. Blood-Horse 34, 22–23. Wilsher, S., and Allen, W. R. (2003). The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet. J. 35, 476–483. doi:10.2746/042516403775600550 Wilsher, S., Allen, W. R., and Wood, J. L. N. (2006). Factors associated with failure of thoroughbred horses to train and race. Equine Vet. J. 38, 113–118. doi:10.2746/042516406776563305
www.publish.csiro.au/journals/rfd
Review
Reproduction, Fertility and Development, 2015, 27, 872–879 http://dx.doi.org/10.1071/RD14390
Not just a number: effect of age on fertility, pregnancy and offspring vigour in thoroughbred brood-mares Charles F. Scoggin Claiborne Farm, PO Box 150, Paris, KY 40362, USA. Email: [email protected]
Abstract. Advancing age can adversely affect a thoroughbred brood-mare’s reproductive efficiency and influence the commercial and athletic potential of her progeny. Causes for the decline in fertility include decreased oocyte and embryo quality, anatomical defects and endometrial degeneration. In addition, evidence exists that as the age of a dam increases, her foals will be at increased risk of morbidity and mortality during the neonatal period. Health issues can have lasting and deleterious effects on surviving foals, including decreased sale value and reduced athletic performance. The purpose of this review is to evaluate the association between mare age, fertility and offspring vigour in thoroughbred horses. Additional keywords: maternal age, offspring health, subfertility. Received 13 October 2014, accepted 17 February 2015, published online 19 March 2015
Introduction Contrary to a contemporary aphorism, age is, indeed, more than a number as it pertains to reproductive efficiency and offspring vitality in thoroughbred horses. The correlation between advancing age and declining fertility is a phenomenon fairly ubiquitous among domestic animals. In food animals, this corollary leads to regular culling of older animals and replacement with younger animals. Doing so is done for both economic and management reasons, such as improving herd fertility rates, increasing genetic diversity or exploiting a certain phenotype. Horses offer a unique contrast to other livestock when it comes to selection of breeding stock. First, the primary function of horses is that of athletic performance and recreation, not food or fibre production; thus, less emphasis is placed on fertility when selecting breeding stock. Second, the commercial value of individual horses often far exceeds that of other farm animals and money spent towards obtaining a single live foal can extend into the tens, if not hundreds, of thousands of dollars when factoring in stud fees and labour. A third distinction is that owners place a significant amount of sentimental value on their horses. There is a large contingent of equestrians who consider their horses to be pets, or even immediate members of their families, and not farm animals. Fourth, the gestation length of horses is longer than most other domestic animals. When coupled with an extended gap from birth to the onset of training (,2 years), several years, and hence several foal crops, are needed to determine the worthiness of a sire or dam as producers of quality offspring. As it relates specifically to North American thoroughbreds, breeding and registration requires strict adherence to the rules and regulations set forth by The Jockey Club (http://www.registry. jockeyclub.com/registry.cfm?Page=tjcRuleBook, accessed 3 Journal compilation Ó CSIRO 2015
March 2015). The one notable and rather unique (compared with other breed registries) requirement for registration is that all thoroughbreds must be conceived via the act of live cover. This rule precludes the use of any assisted reproductive technique (ART), whether it is artificial insemination, embryo transfer or other in vitro methods of fertilisation, such as intracytoplasmic sperm injection. The consequences of this rule are numerous and far-reaching, particularly as it relates to reproductive management of thoroughbred brood-mares. Not only must mares conceive and carry a foal to term, but they must also do so with regularity to remain profitable. What is more, most commercial thoroughbred breeders will continue to breed aged animals well beyond their reproductive prime, especially those that are proven producers of quality blood stock. Interestingly, and contrary to this notion, there are several scientific studies that suggest younger mares are more likely to produce quality offspring as opposed to their older counterparts (Finocchio 1985; Lema and Finocchio 1985; Barron 1995; Morley and Townsend 1997). Economic analyses and certain observational studies offer intriguing viewpoints regarding the commercial value and productivity, in terms of both economic and athletic performance, of offspring of older mares. Certain accounts demonstrate that even the most blue-blooded of mares will only produce one high-quality individual in her lifetime (Finocchio 1985), whereas others point out notable exceptions to this observation, thereby spurring the desire to breed older mares in an attempt to catch lighting in a bottle one more time (Consignors 2007). As discussed below, there is a significant association between mare age and various reproductive measures. The consequences of aging are multifactorial and often cumulative, whereas the fallouts of breeding older mares have both direct www.publish.csiro.au/journals/rfd
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Table 1. Measures of reproductive performance in brood-mares, adapted from Nath (2011) and Ginther (1993) Pregnancy rate per cycle First cycle pregnancy rate Seasonal pregnancy rate Live-foal rate Embryonic loss rate Fetal loss rate Abortion rate Services per pregnancy Cycles per pregnancy
Percentage of mated mares that are pregnant on a specified day after mating Percentage of mares that are pregnant after the first mated oestrus Percentage of mares that are pregnant at the end of the breeding season Percentage of mated mares that produce a live foal Percentage of fertilised oocytes that do not survive to 42 days after mating Percentage of pregnancies surviving to 42 days that do not result in a live foal General term regarding pregnancy loss that needs to be defined in relation to stage of gestation Number of times a mare is served before diagnosis of pregnancy Number of served oestrous cycles before the mare becomes pregnant in one season
and indirect effects on them and their offspring. Most notably, these effects can influence the commercial value of the mare, as well as the future value of a foal as either a commodity or athlete. How old is too old? Before attempting to answer this question, it is important first to define certain parameters used to quantify reproductive efficiency in brood-mares. As adapted from Ginther (1993) and recently described by Nath (2011), commonly used measures are listed in Table 1. Hereto forth, when describing the day of pregnancy and gestation, that day will be in reference to the day of the last mating, which is defined as Day 0. Not surprisingly, there is no hard and fast rule for the age at which mares will experience a decline in fertility. This age varies among individuals, farms and locales. Nevertheless, a review of the literature clearly demonstrates that age is one of the most consistent factors dictating a mare’s reproductive capacity. An early report from the US indicated that seasonal pregnancy rates started to decline gradually in mares aged 13 years and older (Hutton and Meacham 1968). More recent reports from central Kentucky, USA (Baker et al. 1993; Bosh et al. 2009a), Newmarket, UK (Morris and Allen 2002; Allen et al. 2007), and Victoria, Australia (Bru¨ck et al. 1993; Nath 2010), scrutinised this phenomenon further by evaluating several different reproductive parameters from data collected from regional stud farms. As indicated in Table 2, when mares were divided into certain age groups, early (Day 15–21) per cycle pregnancy rates began to wane, on average, when mares reached 14 years of age. Day 40–42 per cycle pregnancy rates for the US and UK appeared to decline at an even earlier age (Table 3), and data from both countries demonstrate a progressive drop with advancing age groups. With respect to embryonic death rates (defined as early detection of a pregnancy followed by loss at or before 42 days gestation), equivocal results were reported among the different studies in that the ages at which a significant interaction occurred varied between different regions (Table 4). Regardless, the incidence escalated with increasing age, with the youngest group of mares having the lowest frequency of embryonic death. It was intriguing to observe that the study from Australia (Nath 2010) reported an embryonic loss rate of 11.8% in mares aged .18 years. This value appears to be substantially lower than values from studies out of central Kentucky (23.1%; Bosh et al. 2009a) and Newmarket (18.6%; Allen et al. 2007). The
Table 2. Early (approximately Days 15–21) per cycle pregnancy rates for thoroughbred brood-mares grouped by age in various regions of the world Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) Age (years) 2–8 9–13 14–18 .18
USA
UKB
AustraliaC
66.3%a 65.6%a 61.0%ab 48.1%b
67.3%a 63.4%a 58.3%b 54.9%b
72.1%a 69.8%a 61.7%b 55.0%b
A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007). C Adapted from Nath (2010). B
Table 3. Day 40–42 per cycle pregnancy rates for thoroughbred brood-mares grouped by age in the US and UK Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) USA
UKB
63.2%a 59.0%a,b 50.8%bc 37.0%c
63.0%a 58.5%b 52.0%c 43.8%d
Age (years) 2–8 9–13 14–18 .18 A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007).
B
Table 4. Embryonic death rates for thoroughbred brood-mares grouped by age in various regions of the world Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) Age (years) 2–8 9–13 14–18 .18 A
USA
UKB
AustraliaC
4.6%a 10.1%a,b 16.7%b 23.1%b
5.9%a 7.1%a 10.0%b 18.6%c
5.1%a 7.9%b 10.0%b 11.8%b
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007). C Adapted from Nath (2010). B
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Table 5. Seasonal Day 40–42 pregnancy and live-foal rates in thoroughbred brood-mares grouped by age in the US and UK Within columns, values with different superscript lowercase letters differ significantly (P , 0.05) USA
Age (years) Day 40 (%) 2–8 9–13 14–18 .18
a
93.7 90.2a 80.9b 67.2b
UKB
Live-foal (%) a
82.9 80.1a 68.4b 55.2b
Day 42 (%) a
91.2 87.9b 83.5c 73.6d
Live-foal (%) 81.8a 76.8b 73.1b 62.8c
A
Adapted from Bosh et al. (2009a). Adapted from Allen et al. (2007).
B
reasons for this perceived discrepancy are not immediately known, but may be due to differences in reproductive management, mare status and stallion fertility. Moreover, fetal loss and live foal rates were not reported in the study of Nath (2010) as they were in the other studies, which, if available, would help better elucidate the disparity in results. Age also significantly impacts seasonal pregnancy and livefoal rates (Table 5). In central Kentucky, both these measures were similar between mares aged 2–8 and 9–13 years of age, but decreased significantly in the two older age groups (14–18 years and .18 years). In Newmarket, Day 42 pregnancy rates decreased with each successive age group. In addition, the youngest group of mares had higher live-foal rates than the other groups. Predictably, mares aged .18 years had significantly lower live-foal rates compared with the other age groups. Differences in these results could be related to difference in sample sizes between the two studies. Bosh et al. (2009a) tallied records from a total of 1011 mares over 1559 oestrous cycles, whereas Allen et al. (2007) had over threefold as many mares and cycles, which likely improved statistical power and reduced the likelihood of Type II errors. In contrast with the previously discussed studies, a report out of Sweden (Hemberg et al. 2004) found that mare age did not have a significant effect on per cycle pregnancy rates. However, these researchers used different age groupings, with the oldest group comprising mares .13 years of age. Furthermore, they did find a significant association between increasing age and increasing pregnancy loss and decreasing live-foal rates, findings that are in agreement with other studies from central Kentucky (Baker et al. 1993; Bosh et al. 2009a), Newmarket (Morris and Allen 2002; Allen et al. 2007) and Victoria (Bru¨ck et al. 1993; Nath 2010). A final observation pertains to the relative intensity of management as the age of a mare increases. For example, Allen et al. (2007) reported that mares 9 years of age or older required more covers to obtain a Day 15 pregnancy than younger mares. They also demonstrated a significant increase between groups in the percentage of mares given uterine treatments. The implications of these findings are that older mares require more intensive veterinary management, which translates into more time, resources and money needed to obtain a pregnancy. The aforementioned studies provide strong evidence that as the age of a thoroughbred mare increases, her reproductive
efficiency decreases. This decrease is manifested in declining pregnancy rates (both per cycle and seasonal) and live-foal rates, as well as increased embryonic and fetal loss rates. In addition, there is some evidence supporting the notion that the incidence of embryonic loss appears to increase sooner, with respect to age, than per cycle and seasonal pregnancy rates in mares. This finding could influence future management strategies in that certain proactive measures (e.g. more aggressive pre- and postbreeding management, routine and serial pregnancy examinations, progesterone supplementation and vulvoplasties) could be taken to reduce the risk of embryonic and fetal loss in relatively young mares. However, and as mentioned previously, increasing the intensity of management can lead to increasing expenses to produce a pregnancy and generate a live foal. Age-related factors affecting reproductive efficiency The causes for the association between increasing mare age and the decline in fertility are numerous and multifactorial. Examples include reduced oocyte and embryonic viability, degenerative changes to the external and internal reproductive tract and changes in the development of fetal membranes. These factors are not mutually exclusive and can occur in tandem to cause reductions in the various measures of reproductive efficiency discussed above. Scientific studies have provided sound evidence of the association between declining oocyte viability and advancing mare age. Using oocyte transfer (OT), Carnevale and Ginther (1995) showed that oocytes from older donor mares resulted in significantly fewer pregnancies than those from younger donor mares when oocytes were transferred into young recipient mares. Advancing age has also been postulated as being the primary determinant for the relative success (or lack thereof) of obtaining pregnancies from older mares in a commercial OT program (Carnevale et al. 2001). Reduced oocyte quality, and hence decreased pregnancy rates, in older mares may be due to age-related morphological differences in oocytes. Increased vacuolisation of and changes in the shape of oocytes were more commonly seen in older compared with younger mares when both light and electron microscopy were used to evaluate oocytes from mares of different ages (Carnevale et al. 1999). Using a clinical grading system based on cumulus cell expansion and the appearance of the ooplasm, oocytes from mares $20 years of age had poorer morphological grades compared with younger mares (Carnevale et al. 2005). More recently, Rambags et al. (2006, 2014) demonstrated a reduced quantity of mitochondria in in vitro-matured oocytes from older compared with younger mares. They also used transmission electron microscopy to reveal morphological changes in mitochondria from oocytes of older mares, such as swelling and loss of internal architecture. These studies have immediate practical considerations. Changes seen in oocytes of older mares could alter the complex and highly energy-dependent events involved in oocyte maturation, thereby leading to a reduction in oocyte viability. As a result, embryo developmental rates could be negatively affected, ultimately resulting in reduced pregnancy rates and/or increased embryonic loss more commonly seen in aged mares (Ball et al. 1989; Ball 2011). Embryo transfer of Day 4 embryos
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collected from old, subfertile donors into normal recipients yielded significantly lower Day 14 pregnancy rates compared with transfer of embryos from young, normal donors (Ball et al. 1989). In addition, Carnevale et al. (1993) reported smaller embryonic vesicle sizes and lower Day 11 pregnancy rates in old mares relative to young mares. Differences in morphological embryonic development rates between young and old mare donors has also been documented, with embryos collected from older donors and cultured in vitro having more microscopic abnormalities than those from younger mares (Brinsko et al. 1994). Changes in the quality and character of the embryo may be a result of aneuploidy, which could account for a significant portion of early embryonic loss in brood-mares. Previous work by Ball et al. (1989) showed that despite relatively high early (Day 4) pregnancy rates, embryonic development was either delayed or lower in embryos transferred from older mares during subsequent pregnancy examinations. Derangements in chromosomal structure and DNA replication can alter proper development of human embryos, and the rate of aneuploidy has been shown to increase with increasing age in women (Nagaoka et al. 2012). This phenomenon has not been thoroughly investigated in the horse, but it likely represents a realistic means for the increased frequency of embryonic loss seen in older mares. Anatomically, one of the most well-documented changes in thoroughbred brood-mares is worsening of perineal conformation with age. First described by Caslick (1937), poor vulvar conformation was most commonly seen in older multiparous mares and was shown to adversely affect reproductive performance. The effect on fertility is related to aspiration of air and faecal contents into the vagina, which causes inflammation and colonisation of bacteria in the reproductive tract, including the uterus. The most common clinical presentation is a decreased angle of declination of the vulva with respect to the horizontal plane, a shortened vulva and a sunken anus. Treatment typically entails performing a Caslick vulvoplasty (also known as ‘Caslick’, ‘vulvoplasty’ or ‘suture’). The need for this surgery can be determined by calculating the Caslick index as described by Pascoe (1979); however, most practitioners will forgo the calculation and instead perform the procedure in mares with a history of subfertility. Agreement generally exists among theriogenologists that once a mare has a vulvoplasty, she will require one during successive pregnancies (Bradecamp 2011). In thoroughbred foaling mares, a vulvoplasty is usually performed within a week after foaling. The benefits include reducing the severity of endometritis, as well as improving first cycle pregnancy rates and live-foal rates. A study evaluating vulvar conformation and its relationship to endometrial cytology and fertility in thoroughbred mares underscored the importance of maintaining a vulvoplasty during subsequent pregnancies (Hemberg et al. 2005). Mares that were not re-sutured after parturition had a significantly higher incidence and increased severity of endometritis compared with mares that were sutured shortly after foaling. The former group also had significantly lower first-cycle pregnancy and live-foal rates compared with the latter group, further emphasising the importance of performing a vulvoplasty in a timely manner after foaling.
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No matter how well managed a mare is, she will, with advancing age, develop progressive changes to her endometrium (Rickets and Alonso 1991). These changes are associated with lower live-foal rates (Kenney 1978). Inflammatory cell infiltrates, glandular fibrosis and nesting and lymphangiectasia are common histopathological findings that, when combined with a history of subfertility, comprise the disease complex known as chronic degenerative endometritis (CDE; Allen 1993). Because the relative intimacy of the fetal–maternal interface is extremely influential with respect to nutrient exchange and promoting proper development of the fetus, a possible consequence of CDE is reduced development and efficiency of the fetal membranes. Using light and scanning electron and transmission electron microscopy, Bracher et al. (1996) examined the ultrastructural attachments of the endometrium and allantochorion in normal pregnant mares and pregnant mares with CDE. They were able to discern a delay in and reduction of microcotyledon development in mares with CDE compared with normal mares. More recently, this same laboratory used stereology to examine the impact of age and parity on fetal membrane development for term pregnancies (Wilsher and Allen 2003). Their results demonstrated that the surface density of the microcotyledons was significantly lower in multiparous mares 16 years of age or older compared with younger primaparous and multiparous mares. Thus, there is a possibility that differences in the development of equine fetal membranes seen in older mares could increase the risk of fetal growth retardation and/or fetal demise. This notion also corresponds with the longheld belief among some thoroughbred breeders that mares tend to have skinnier and poorer looking foals later in life, hence spawning the colloquial term ‘old mare foal’. However, the scientific evidence suggests otherwise, because neither the efficiency of fetal membranes nor foal birthweights were significantly reduced in older compared with younger mares (Wilsher and Allen 2003). These results were confirmed in a more recent report and parity was instead shown to be the primary factor influencing foal birthweight in that for every extra foaling, birthweight increased by 0.8 kg (Elliott et al. 2009). Despite these conflicting results, it would be a mistake to discount the effect of mare age on fetal development, the reason being the intimate link between age and parity. Not only do most thoroughbred brood-mares start their reproductive careers at a relatively young age (3–6 years of age), but they must also carry their pregnancies to term. Thus, age and parity are almost inseparable and enjoy a synergistic relationship with respect to reproductive efficiency in thoroughbred mares. The author is aware of the potential for confounding results when the two are not separated (Elliott et al. 2009), but will not henceforward quibble over the distinction. Advancing mare age and its influence on offspring vigour and value One of the primary objectives of thoroughbred breeders is to raise horses in a manner that allows them to realise their full athletic potential. Thoroughbred breeding is also big business
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and the money involved at public auctions generates added pressure on breeders and consignors to present a commercially appealing product. Producing a quality athlete and/or marketable prospect involves a confluence of factors, with mare age being a polemical element involved in achieving success in the thoroughbred industry. As discussed below, advancing mare age not only has measurable effects on foal health, performance and profit, but it can also introduce bias against the relative commercial value of both a dam and her offspring. The first year of life is one of the more formative times of a horse’s life. Mitigation and management of disease are essential during this phase, because disease can have lasting and potentially disastrous consequences on athletic performance. For example, bacteraemic neonatal foals have been shown to have fewer wins and total earnings than maternal siblings (Sanchez et al. 2008). Morley and Townsend (1997) demonstrated the negative impact of foal illness on commonly sought-after physical attributes for racing performance. Sick neonates (#14 days of age) were fivefold more likely to be considered unsuitable as equine athletes assuming they reached 1 year of age, whereas foals between the ages of 15 days and 1 year experiencing health issues were sevenfold more likely to be deemed unacceptable for athletic performance at 1 year of age. Morley and Townsend (1997) also identified increasing mare age as a major risk factor for morbidity and mortality in both neonates and foals between the ages of 15 days and 1 year. The average age for dams of foals experiencing health issues (11.4 years) or dying during the neonatal period (12.4 years) was significantly higher than for dams of foals not experiencing health problems (10.6 years) or surviving to 15 days of life (10.6 years). In addition, the mean age of mares with foals that died between 15 days and 1 year (13.1 years) was higher than that of mares with foals that survived past 1 year of age (10.6 years). Angular limb deformities (ALD) were cited as the specific health issue that had the highest likelihood of producing an unsatisfactory physical assessment. Causation for the association between mare age and increased risk of foal morbidity and mortality were not immediately evident from that study. Morley and Townsend (1997) did speculate that there may be a link between endometrial degeneration and foal illness. Altered nutrient exchange and energy partitioning could adversely affect fetal development and certain parturient events (e.g. colostrum production and milk let-down) required for neonatal growth and development. Adverse health events early in life can also impact future athletic ability. For racehorses, speed ratings are commonly used measures to express the racing merit of an individual horse. In the UK, Timeform ratings are an example of such a metric. The higher the rating, the better the performance, with superior horses rating at or above 130 and inferior horses in the 50s or lower. To evaluate the effect of mare age and parity on progeny Timeform ratings, a small (n ¼ 81) study was conducted that selected for mares that had at least eight live foals, two of which had obtained a Timeform rating of $110 (Barron 1995). Ratings for offspring peaked at a maternal age of 9 years and declined significantly thereafter. A similar effect of parity on Timeform ratings was seen (i.e. as parity increased, ratings decreased). A more recent and larger (n ¼ 431) study provided somewhat
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opposing results (Wilsher et al. 2006). No significant effect of mare age or parity was observed with respect to the likelihood of progeny running as 2 or 3 year olds, winning a race or performance based on Timeform ratings. However, as Wilsher et al. (2006) point out, their study only considered one offspring per dam, so the differences in study design and sample selection between the two papers may account for the divergent results. Nonetheless, the disparity in outcomes between studies introduces the element of class, another measure of potential and performance, and its relationship with age. ‘Class’ is a term used to describe both tangible and intangible virtues of racehorses that, collectively, serve as an indicator for their relative skill level. Quantitative measures of class are calculated similar to speed ratings and are based primarily on past performances, such as timed work-outs and races. More esoteric indicators of class are pedigree, physical stature, tactical speed, grit and heart. Thus, ‘class’ is a fluid and somewhat amorphous concept that can change throughout an individual racehorse’s career. One of the capstones of class is winning a stakes race. When investigating the progeny performance of 1641 brood-mares who produced 18 931 foals, an astounding 11.5 foals per mare, Finocchio (1985) reported that 14.5% of these foals became stakes winners. Also of note was the fact that 43.3% of these mares produced more than one stakes winner. When factoring in age and parity, stakes-producing ability declined in a nearly linear fashion after 7 years of age and the likelihood of producing a stakes winner waned progressively beginning with the sixth parity. Statistical analyses of these data revealed that mares #10 years of age produced a greater proportion of stakes winners than those aged .10 years. When evaluating birth ranks (i.e. the order in which a foal was born from an individual mare), a larger proportion of foals with birth-ranks ,6 were stakes winners compared with foals with higher birth-ranks (Lema and Finocchio 1985). When taken as a whole, these results provide testimony to the perception within the thoroughbred breeding business that class begets class. Unfortunately, and as most breeders and owners would attest to, there is no ‘sure thing’ when it comes to breeding for performance and profit. The element of uncertainty looms large in thoroughbred breeding, thereby making it a stochastic or unpredictable process. The inexact nature of equine reproduction has been shown to have direct consequences on economic returns and profitability. As demonstrated by Bosh et al. (2009b), brood-mares are long-term investments with positive gains dependent on their reproductive efficiency over the course of several years. Profits and rates of return were greatest for maiden mares that produced a registered foal for seven consecutive years before being sold or those that were bred for 9 years and only barren one time 4 years into their production history. Not surprisingly, these researchers identified increasing mare age as a significant factor that limited the odds of producing a registered foal and, summarily, a positive financial yield. Thus, mares should start their reproductive careers early and remain consistently productive. Doing so optimises the likelihood of producing a viable foal and reaping a positive investment. Economic analyses of yearling thoroughbred public auctions illustrate the importance of mares maintaining satisfactory reproductive efficiency and producing quality offspring. In an
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early study by Commer (1990), the month of birth was shown to influence the amount buyers were willing to spend on yearlings. Those that foaled in January and February of the previous year were estimated to sell for almost US$2000 more than yearlings born in May or June. The preference of buyers for older yearlings was confirmed and expanded a few years later, in which yearlings born in January–March fetched significantly higher prices than those born in later months (Buzby and Jessup 1994). When the age of the yearlings was measured in days between foaling and the first day of the auction, Chezum and Wimmer (1997) described a significant association between increasing yearling age and sale price. Finally, when examining quantifiable determinants of auction prices in thoroughbred yearlings over a 13-year period, researchers calculated that yearlings born after April were worth 30% and 18% less than those born in January–February and March–April, respectively (Robbins and Kennedy 2001). The measurable preference for older yearlings is likely due to their physical maturity. Precocity is a highly sought after trait that can translate into successful racing performance as 2 or 3 year olds. Therefore, it behoves commercial breeders to have mares foal early and often to generate precocious offspring, which helps maximise revenue. The Keeneland November Breeding Stock Sale, Lexington, Kentucky, USA is the largest thoroughbred sale of its kind in the world. Econometric studies have been useful when evaluating factors influencing the thoroughbred brood-mare market. Analyses of the summary statistics from past sales identified reproductive efficiency and age as major elements influencing the commercial value of all brood-mares sold. For the 1996 sale, Neibergs (2001) calculated that barren mares had a marginal value discount of US$15 010 stemming from increased production costs in maintaining an open mare and increased risk of poor reproductive soundness. Based on an average age of 9 years, Neibergs (2001) also found that brood-mares lose US$3051 in value for each additional year of age relative to the mean. When studying hammer prices from the 2005 sale, Maynard and Stoeppel (2007) chose to exclude barren mares from their analysis. Removing this particular group was thought to eliminate inherent differences between these two groups of mares, which could have potentially confounded results in the study of Neibergs (2001). Consequently, Maynard and Stoeppel (2007) determined that each additional year of a brood-mare’s age dropped her value by nearly US$12 000. Inflation no doubt played a role in the relative discounts of price attributed to age between these studies, yet there is no ignoring the importance of age when determining the relative commercial value of a broodmare. The age of the mare reflects her potential future earnings from foal production. The younger the mare, the more foals she is capable of producing, thereby increasing her chances of being a successful producer. Ageism: perception versus reality On the surface, culling older mares and selecting offspring from young, healthy mares seems like a practical and financially sound method to breed, raise and race thoroughbreds. Because age is one of the few variables that can actually be controlled for, using this parameter to decide when and which mare to cull
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could be seen as a shrewd method of management. Ageism, some thoroughbred industry analysts would argue, can effectively strengthen the odds of obtaining a top class equine athlete. In his landmark report, Dink (1990) reported that of 137 184 foals to race, 4804 (3.50% overall) were stakes winners and the highest percentage of stakes winners were out of mares that were 4–10 years of age (3.87%). The percentage gravitated mostly downwards from there; mares aged 11–15 years produced 3.32% stakes winners, whereas those aged 16–20 years produced 2.33% stakes winners. Both Rogers (2014) and Tapp (2014) evaluated summary statistics from the 2002–11 Keeneland September Yearling Sales to calculate the average class performance index (CPI) of graduates from this sale. The CPI is used to rank runners by their average earnings per start compared with age- and sex-matched peers. There was a steady downward trend in CPI after a mare’s third foal (Tapp 2014). Another interesting tendency was observed when foal count was charted as a function of average sale price and CPI. As described by Rogers (2014), the average sale price of a mare’s first six foals roughly followed a similar path of the average CPI for these foals. By the seventh foal, there was a precipitous drop in average CPI. Conversely, the average sale price actually increased with the seventh foal. This phenomenon was possibly related to buyers paying a premium for either yearlings out of proven mares or residual bloodstock value of a filly. Nevertheless, if the goal was to purchase a solid racing prospect, paying this premium effectually placed the buyers at a disadvantage when attempting to recoup costs of the purchase due to the likelihood of paying more for a lesser product based on these analytics. As mentioned previously, culling and selection based on age seem commonsensical, especially considering the favourable results obtained when using such a criterion in other livestock species. But, when comparing and contrasting different factors, it is not without its problems. The low cull value of a mare coupled with the high cost of a replacement makes such a practice in mares less economically viable than in other species (Bosh et al. 2009b). Selection based on age also does not translate into guaranteed success on the racetrack, for there are plenty of examples of top class racehorses produced out of older mares. From 1984 to 2006, there were 15 Breeder’s Cup Champions that were out of mares older than 16 years of age (Consignors and Commercial Breeders Association 2007). Then, there is the individual example of the prolific Somethingroyal who was 18 years old when she foaled the immortal and unequalled Secretariat and produced two more stakesplaced horses at 19 and 20 years of age. Somethingroyal is obviously an exception to the rule that age adversely affects fertility and offspring vigour, but she is an unmistakable exception nonetheless. Her produce record serves as a reminder that mares can age and produce at different rates due to a conflux of both genetic and environmental factors, thereby giving breeders pause when contemplating culling an older mare from a breeding program. In addition, it would be contemptuous of us clinicians to ignore the emotional value of brood-mares. Some of these mares may represent an owner’s first winner or a family’s breeding legacy, which contributes added yet immeasurable value to the mare above and beyond her market price.
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Finally, ageism in thoroughbreds may represent a sublime Darwinian concept or a surreptitious method to improve the breed. The requirement that all foals must be conceived via the act of live-cover and carried to term by their dam selects for fertility to a much greater extent than what is seen in other breeds that allow the use of ART. Further, if an aged mare has maxed out her potential as a quality producer, her offspring will be a reflection of such, effectively removing her from both the commercial market and the breeding population. Thus, it seems that ageism is both perception and reality, which represents a microcosm of the racing industry itself. Attempting to establish a set formula guaranteeing success is impossible, if not unrealistic, to attain due to a legion of prominent and, at times, paradoxical factors. However, thoroughbred breeding can be lucrative, with the economic impact in central Kentucky alone estimated to be in the billions of dollars (Kentucky Horse Council 2013). When combined with the allure and lustre of owning and racing elite equine athletes, the motivation will likely always exist to search for a sweeping edict securing prosperity in this industry. Conclusions As judged by pregnancy, embryonic loss and live-foal rates, advancing mare age can adversely affect reproductive efficiency. Neonatal vigour also appears to be dependent on the age of the dam in that foals from older mares appear more prone to morbidity and mortality than those out of younger mares. Evidence exists for an association between athletic performance of the progeny and mare age, but this relationship likely works in synergy with parity. Similarly, the commercial value of either a mare or her produce can be affected by age and parity, although buyers are willing to pay a premium for offspring from older mares despite increased risks of diminished returns on their investment. Mare age has a complicated and perplexing relationship within the thoroughbred industry. As researchers and clinicians, we should continue to explore this relationship to help evolve the industry and sustain the welfare of its most precious commodity, the horse. References Allen, W. R. (1993). Proceedings of the John P. Hughes International Workshop on Equine Endometritis. Equine Vet. J. 25, 184–193. Allen, W. R., Brown, L., Wright, M., and Wilsher, S. (2007). Reproductive efficiency of Flatrace and National Hunt thoroughbred mares and stallions in England. Equine Vet. J. 39, 438–445. doi:10.2746/ 042516407X1737581 Baker, C. B., Little, T. V., and McDowell, K. J. (1993). The live foaling rate per cycle in mares. Equine Vet. J. Suppl. 25(S15), 28–30. Ball, B. A. (2011). Embryonic loss. In ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2327–2336. (Wiley-Blackwell: Ames, IA.) Ball, B. A., Little, T. V., Weber, J. A., and Woods, G. L. (1989). Survival of Day 4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J. Reprod. Fertil. 85, 187–194. doi:10.1530/JRF.0.0850187 Barron, J. K. (1995). The effect of maternal age and parity on the racing performance of thoroughbred horses. Equine Vet. J. 27, 73–75. doi:10.1111/J.2042-3306.1995.TB03036.X
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Bosh, K. A., Powell, D., Shelton, B., and Zent, W. (2009a). Reproductive performance measures among thoroughbred mares in central Kentucky, during the 2004 mating season. Equine Vet. J. 41, 883–888. doi:10.2746/ 042516409X456068 Bosh, K. A., Powell, D., Neibergs, J. S., Shelton, B., and Zent, W. (2009b). Impact of reproductive efficiency over time and mare financial value on economic returns among thoroughbred mares in central Kentucky. Equine Vet. J. 41, 889–894. doi:10.2746/042516409X456059 Bracher, V., Mathias, S., and Allen, W. R. (1996). Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Equine Vet. J. 28, 180–188. doi:10.1111/J.2042-3306.1996. TB03771.X Bradecamp, E. A. (2011). Pneumovagina. In ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2537–2544. (Wiley-Blackwell: Ames, IA.) Brinsko, S. P., Ball, B. A., Miller, P. G., Thomas, P. G. A., and Ellington, J. E. (1994). In vitro development of Day 2 embryos obtained from young, fertile mares and aged, subfertile mares. J. Reprod. Fertil. 102, 371–378. doi:10.1530/JRF.0.1020371 Bru¨ck, I., Anderson, G. A., and Hyland, J. H. (1993). Reproductive performance of thoroughbred mares on six commercial stud farms. Aust. Vet. J. 70, 299–303. doi:10.1111/J.1751-0813.1993.TB07979.X Buzby, J. C., and Jessup, E. L. (1994). The relative impact of macroeconomic and yearling-specific variables in determining thoroughbred yearling price. Appl. Econ. 26, 1–8. doi:10.1080/00036849400000055 Carnevale, E. M., and Ginther, O. J. (1995). Defective oocytes as a cause of subfertility in old mares. Biol. Reprod. Mono. 1, 209–214. Carnevale, E. M., Griffin, P. G., and Ginther, O. J. (1993). Age-associated subfertility before entry of embryos into the uterus of mares. Equine Vet. J. 25, 31–35. doi:10.1111/J.2042-3306.1993.TB04820.X Carnevale, E. M., Uson, M., Bozzola, J. J., King, S. S., Schmitt, S. J., and Gates, H. D. (1999). Comparison of oocytes from young and old mares with light and electron microscopy. Theriogenology 51, 299. doi:10.1016/S0093-691X(99)91858-7 Carnevale, E. M., Squires, E. L., Maclellan, L. J., Alvarenga, M. A., and Scott, T. J. (2001). Use of oocyte transfer in a commercial breeding program for mares with reproductive abnormalities. J. Am. Vet. Med. Assoc. 218, 87–91. doi:10.2460/JAVMA.2001.218.87 Carnevale, E. M., Coutinho da Silva, M. A., Panzani, D., Stokes, J. E., and Squies, E. L. (2005). Factors affecting the success of oocyte transfer in a clinical program for subfertile mares. Theriogenology 64, 519–527. doi:10.1016/J.THERIOGENOLOGY.2005.05.008 Caslick, E. A. (1937). The vulva and the vulvo–vaginal orifice and its relation to genital health of the thoroughbred mare. Cornell Vet. 27, 178–187. Chezum, B., and Wimmer, B. (1997). Roses or lemons: adverse selection in the market for thoroughbred yearlings. Rev. Econ. Stat. 79, 521–526. doi:10.1162/REST.1997.79.3.521 Commer, M. (1990). The effect of non-phenotypic data on thoroughbred prices in the mid-Atlantic market. Prof. Anim. Sci. 7, 18–24. Consignors and Commercial Breeders Association (2007). Myth #3: foals out of older mares. In: ‘Buying Sales Yearlings: Plain and Simple’. (Eds R. Manseau.) pp. 24–25. (The Conignors and Commercial Breeders Association: Lexington, KY.) Kentucky Horse Council (2013). ‘2012 Kentucky Equine Survey.’ (University of Kentucky Ag Equine Programs: Lexington, KY.) Dink, D. (1990). Advantages of a February foal. Thoroughbred Times May 4, 28–32. Elliott, C., Morton, J., and Chopin, J. (2009). Factors affecting foal birth weight in thoroughbred horses. Theriogenology 71, 683–689. doi:10.1016/J.THERIOGENOLOGY.2008.09.041 Finocchio, E. J. (1985). Race performance and its relationship to birthrank and maternal age – I. In: ‘Proceedings From the 31st Annual Convention
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Nath, L. C. (2011). Reproductive efficiency. In: ‘Equine Reproduction’, 2nd edn. (Eds A. O. McKinnon, E. L. Squires, W. E. Vaala and D. D. Varner.) pp. 2779–2789. (Wiley-Blackwell: Ames, IA.) Neibergs, J. S. (2001). A hedonic price analysis of thoroughbred broodmare characteristics. Agribusiness 17, 299–314. doi:10.1002/AGR.1017 Pascoe, R. R. (1979). Observations on the length and the angle of declination of the vulva and its relation to fertility in the mare. J. Reprod. Fertil. Suppl. 27, 299–305. Rambags, B. P. B., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2006). Oocyte mitochondrial degeneration during reproductive ageing in the mare. Havemeyer Found. Monogr. Ser. 18, 25–27. Rambags, B. P., van Boxtel, D. C. J., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. E. (2014). Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81, 959–965. doi:10.1016/ J.THERIOGENOLOGY.2014.01.020 Ricketts, S. W., and Alonso, S. (1991). The effect of age and parity on the development of chronic endometrial disease. Equine Vet. J. 23, 189–192. doi:10.1111/J.2042-3306.1991.TB02752.X Robbins, M., and Kennedy, P. E. (2001). Buyer behavior in a regional thoroughbred yearling market. Appl. Econ. 33, 969–977. doi:10.1080/ 00036840010002529 Rogers, B. (2014). Ageism at yearling sales. Bluebloods September, 37. Sanchez, L. C., Giguere, S., and Lester, G. D. (2008). Factors associated with survival of neonatal foals with bacteremia and racing performance of surviving thoroughbreds: 423 cases (1982–2007). J. Am. Vet. Med. Assoc. 233, 1446–1452. doi:10.2460/JAVMA.233.9.1446 Tapp, I. (2014). Young mares. Blood-Horse 34, 22–23. Wilsher, S., and Allen, W. R. (2003). The effects of maternal age and parity on placental and fetal development in the mare. Equine Vet. J. 35, 476–483. doi:10.2746/042516403775600550 Wilsher, S., Allen, W. R., and Wood, J. L. N. (2006). Factors associated with failure of thoroughbred horses to train and race. Equine Vet. J. 38, 113–118. doi:10.2746/042516406776563305
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