- Email: [email protected]
Reproductive efficiency of Thoroughbred mares under Indian subtropical conditions: A retrospective survey over 7 years
Animal Reproduction Science 117 (2010) 241–248
Contents lists available at ScienceDirect
Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Reproductive efficiency of Thoroughbred mares under Indian subtropical conditions: A retrospective survey over 7 years夽 Sumeet Sharma a,∗ , G.S. Dhaliwal b , Dinesh Dadarwal c,1 a
Civil Veterinary Hospital, Mahatam Nagar, Fazilka, Punjab 152 123, India Department of Veterinary Clinical Services Complex, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, Punjab 141004, India c Department of Animal Reproduction, Gyanecology and Obstetrics, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, Punjab 141004, India b
a r t i c l e
i n f o
Article history: Received 18 September 2008 Received in revised form 4 May 2009 Accepted 14 May 2009 Available online 21 May 2009 Keywords: Mare Reproductive efficiency Pregnancy loss Summer stress Embryonic mortality
a b s t r a c t Service records of 253 mares (1181 mare-years) spanning over 7 consecutive years, from nine organized Thoroughbred stud farms, situated in the subtropical northwestern India were retrospectively analyzed to assess their reproductive performance. The overall per cycle pregnancy rate at Day 16 and overall foaling rates were 50.30% and 68.95%, respectively, and were significantly higher in mares aged 3–7 years than ≥18 years old mares. The late embryonic losses (9.86%) that occurred between Days 16 and 39 post-ovulation contributed more than 50% of the overall detected pregnancy losses (19.11%). The overall percent detected pregnancy losses were lower in mares at ages 3–7 years compared to those at ages ≥18 years (14.78% vs. 46.43%, respectively; P < 0.0001). Chronic barren and habitual aborter mares tended to affect reproductive efficiency of mares. Fifty percent of the mares that experienced ≥2 consecutive abortions or barren years, again stayed aborted or barren in the next seasons, respectively. No effect of numbers of matings per oestrus was observed on overall fertility. Neither the induction of oestrus nor ovulation by exogenous hormonal treatment had any effect on most of the analyzed reproductive parameters. Regarding breeding month or years, the reproductive efficiency did not differ significantly. The incidence of multiple pregnancies was 5.40% and percent late embryonic loses were higher (P = 0.0016) in twin (21.98%) than singleton (8.64%) pregnancies. In conclusion, comparatively lower fertility rates were recorded in Thoroughbred mares bred under Indian subtropical climatic conditions than those reported from temperate regions that might be due to difference in breeding management rather than prevailing environment. © 2009 Elsevier B.V. All rights reserved.
1. Introduction
夽 The present study is a part of the MVSc thesis submitted by the first author to the Department of ARGO, Punjab Agricultural University, Ludhiana, India. ∗ Corresponding author at: Street No. 3, Shakti Nagar, Fazilka, Punjab 152 123, India. Tel.: +91 1638 263330. E-mail address: [email protected] (S. Sharma). 1 Present address: Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, 52 Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, S7N 5B4, Canada. 0378-4320/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2009.05.011
Mares have the lowest fertility rate compared to females of other domesticated species, as horse breeds have been selected based on war, draft and racing abilities rather than fertility (Engelken, 1999). Further, in Thoroughbred horses, pedigree and track records are the highest priority for selecting the best of the breed, and generally overlooks the physiological and managerial factors that might affect reproductive performance during their breeding career. Over the last two decades, retrospective studies on fertility in Thoroughbred mares across the world have revealed per cycle pregnancy rates ranging from 54% to 64% (Brück et
242
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
al., 1993; Allen et al., 2007), while, the cumulative end-ofseason pregnancy rates and foaling rates ranged from 85% to 95% (Morris and Allen, 2002; Hemberg et al., 2004) and 62–83% (Morris and Allen, 2002; Schulman et al., 2003), respectively. For the Thoroughbred mares in northern hemisphere, a 4-month breeding period (February–June) is arbitrarily imposed for the purpose of age-related racing. In northwestern India, mares experience high ambient temperature and increased relative humidity for almost half of the breeding period (mid-April to mid-June). The deleterious effects of summer stress on fertility have been well documented in other farm species (Ju and Tseng, 2004; Marai et al., 2007; Nagamine and Sasaki, 2008). However, no such information in Thoroughbred mares exists to the best of our knowledge. Moreover, in an evolutionary perspective, horses prefer temperate climate (Ginther et al., 2004) and the effect of change of climate on their reproductive performance have not been critically investigated. Thus, we investigated reproductive performance of Thoroughbred mares bred under Indian subtropical conditions. A thorough understanding of factors influencing reproductive efficiency should help to identify mares at greatest risk of pregnancy loss and also to organize breeding management in a way best suited to obtain optimal fertility. 2. Materials and methods 2.1. Database Service records of 253 mares for seven consecutive (1998–2005) breeding seasons (February–June) from nine organized Thoroughbred stud farms of northwestern India (lies between 28◦ 28 and 30◦ 30 N latitude and between 74◦ 31 and 77◦ 02 E longitude) were analyzed. A survey form was prepared and fertility data for the mares was recorded. As the records of the stud farms were confidential, all the stud farms and mares were identified by numerical codes only. 2.2. Groups The mares were grouped according to age (3–7, 8–12, 13–17, ≥18 years), reproductive status, i.e. maiden (never mated), barren (mated without a pregnancy at the end of last breeding season), foaling (foaled in the current season and lactating throughout the season), rested (parous mare deliberately not mated during the last breeding season), aborted (pregnant at the end of last breeding season but lost pregnancy later on and/or did not foal) and repeated (mares rebred again in the same season after losing a detected pregnancy irrespective of previous status and considered as a new mare year). 2.3. Management On all stud farms included in the survey, mares were fed a daily ration according to their reproductive status in a manner that is generally practiced in India
(Lucerne/hay and paddock grass ad libitum plus approximately 5 kg of concentrate divided twice or thrice in a day). Oestrus was monitored daily by teasing, and ultrasonographic/transrectal examination was carried out daily or every other day to follow the dominant follicular development and to confirm ovulation. All the mares were checked by the veterinarian for the follicle size and consistency and thereafter mated with a stallion of acceptable fertility. Mares were mated again at 36–48 h later if the follicle was still present at second examination. In small proportion of mares in which either the ovulation was not monitored after covering or record was unavailable, the day following last mating was assumed as day of ovulation (Day 0). Pregnancy diagnosis was first performed on an average Day 16 post-ovulation, by ultrasonography and/or transrectal palpation and subsequently, on an average Days 21, 32, 39, 50, 65, 90, 135 and 198 postovulation. 2.4. Records The data recorded on the survey forms was analyzed retrospectively after the incomplete individual records had been omitted. Since most of the mares returned to the same stud farm for several years and were bred for more than one breeding season, the terms ‘mare’ and ‘mare-year’ are used synonymously in the rest of the article. Although, original data included 1181 mare-years, but fertility analysis was carried out on 1166 mares after excluding mares that had both of their twin concepti reduced after manual intervention. The reduction with manual intervention by compression was considered successful if the twins were reduced to singleton when examined 3 days later. The pregnancy rates were calculated based on per oestrous cycle (per cycle pregnancy rate Day 16/Day 39) and per season (percentage of mares detected pregnant on Day 16 post-ovulation during the season). However, per cycle pregnancy rate at Day 16 was used for further calculations, it is being synonymously used with Day 16 pregnancy rates. The analyzed pregnancy losses included late embryonic losses occurred between Days 16 and 39, fetal losses from Day 40 post-ovulation to term (early fetal losses—Days 40–90; mid-fetal losses—Days 91–198; late fetal losses—Day 199 to foaling) and overall detected pregnancy losses occurred between Day 16 and foaling. The terms, percent ‘undetected early embryonic mortality (EEM) plus fertilization failure (FF)’ and ‘overall embryonic mortality (EM) plus FF’, were used for the percentage of mares that were detected non-pregnant at Days 16 and 39 post-ovulation, respectively. 2.5. Statistical analysis Statistical analyses were preformed on subpopulation of all the mares with complete information from mating to foaling, about their age, reproductive status, etc. using statistical software Minitab 14 version (Minitab Inc., USA). Chi-squared tests were used to determine if there was an overall effect of each variable on the outcome of interest (Kranzler and Moursund, 1999). If this effect of variable(s) was significant (P < 0.05), multiple
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
243
39 pregnancy rates were recorded in maiden than rested (34.78%) mares. However, the Day 16 pregnancy rates per season were not influenced by the reproductive status of mares (Table 2). Day 16 pregnancy rates in mares that were covered for ≤2 oestrous cycles and ≥3 oestrous cycles in a breeding season were 51.11% and 44.21%, respectively, and the difference was not significant under Bonferroni adjustment. Also, stud farm surveyed, the month and year in which mating occurred had no effect on Day 16 pregnancy rates. Of the total number of mated oestruses, 1597 (80.82%) occurred spontaneously and remaining 379 (19.18%) were induced by treatment with one or combination of frequently used exogenous hormone preparation namely: (i) prostaglandin F2␣ or its natural or synthetic analogues (cloprostenol, dinoprost tromethamine) given IM; (ii) 10 days after withdrawal of orally active progestagen, allyl trenabolone (Regumate® ; Intervet India, Pune, India). There was no significant difference in Day 16 pregnancy rate from matings at spontaneous (49.84%) vs. hormone-induced (52.24%) oestrus. The ovulation occurred spontaneously in 81.28% of reported oestrous periods, while, human chorionic gonadotrophin (hCG; Chorulon® , IV; Intervet India, Pune, India), cloprostenol/dinoprost (Estrumate® IM; Schering Plough Animal Health, NJ, USA;/Lutalyse® IM; Pfizer India Limited, Mumbai, India) and buserelin (Receptal® , IV; Intervet, Pune, India) were administered in 17%, 1% and 0.7% of oestrous periods, respectively, to induce ovulation. Inducing ovulation with exogenously administered hormones had no effect upon Day 16 pregnancy rate compared to that
comparisons were carried out and each comparison was considered significant only after making the Bonferroni adjustment. 3. Results 3.1. Management of the oestrous cycle and pregnancy rates The population distribution of mares on the basis of their age and reproductive status are shown in Tables 1 and 2. A sum total of 1166 mares were mated once or more times during 1976 oestrous periods to give an overall per cycle pregnancy rate at Day 16 of 50.30%, while, overall per cycle pregnancy rate at Day 39 was 45.34%. By the end of the season 994 (85.25%) mares had been diagnosed pregnant at around Day 16 post-ovulation. There were 8 aborters and 11 barren mares, which stayed aborters or barrens, respectively, for at least 2 consecutive years with maximum of four breeding seasons. On excluding these mares, the remaining 1053 mare years (1732 oestruses), had overall Day 16 per cycle pregnancy rate of 53.70%. Age of mare markedly affected both per cycle pregnancy rates at Day 16 and Day 16 pregnancy rates per season, as mares at ages 3–7 and 8–12 years had significantly higher rates than ≥18 years old mares (Table 1). Although, reproductive status of mare did not influence Day 16 pregnancy rates under Bonferroni adjustment at P < 0.003 (Table 2), but, Day 39 pregnancy rates were higher (P < 0.003) in maiden (52.66%) and foaling mares (48.53%) compared to barren mares (37.63%). Additionally, greater (P < 0.003) Day Table 1 Effects of age on measures of reproductive efficiency in Thoroughbred mares. Reproductive parameters
Mare age (years)
Mean (n = 1166)
3–7 (n = 354)
8–12 (n = 497)
13–17 (n = 271)
≥18 (n = 44)
Management of estrus Number of oestrus cycles Number of matings per oestrus (S.D.) Number of matings per Day 16 conception (S.D.)
588 1.50 (0.74) 2.77 (0.67)
830 1.44 (0.65) 2.77 (0.68)
480 1.43 (0.71) 3.16 (0.75)
78 1.47 (0.81) 4.11 (0.93)
1976 1.46 (0.71) 2.89 (0.79)
Pregnancy results Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Day 16 pregnancies per season (%) Un-detected EEM plus FF (%) Late embryonic losses (%) Early fetal losses (%) Mid-fetal losses (%) Late fetal losses (%) Overall EM plus FF (%) Overall fetal losses (%) Overall detected pregnancy losses (%) Mares did not produce a foal (%) Mares produced a live foal (%)
54.08a 50.34a 46.09a 89.83a 10.17a 6.92 a 2.70 3.47a 2.52 16.38a 7.86 14.78a 23.45a 76.55a
51.93ab 46.99ab 42.17ab 86.72ab 13.28ab 9.51a 3.33 4.24a 3.05 21.53ab 9.28 18.79a 29.58ab 70.42ab
45.21bc 39.58b 35.00b 80.07bc 19.93bc 12.44 3.68 6.01 2.33 29.89b 10.14 22.58a 38.01b 61.99b
35.90c 25.64c 19.23c 63.64c 36.36c 28.57b 0.00 20.00b 6.25 54.55c 17.86 46.43b 65.91c 34.09c
50.30 45.34 40.69 85.25 14.75 9.86 3.13 4.72 2.78 23.16 9.26 19.11 31.05 68.95
Values in the same row with different letters (a–c) or lacking a common letter differ significantly: Bonferroni (P < 0.008); S.D. (standard deviation). Day 16 pregnancies per season (%): percentage of mares detected pregnant on day 16 post-ovulation during the season; un-detected early embryonic mortality (EEM) plus fertilization failure (FF) (%): percentage of mares that were detected non-pregnant on Day 16 post-ovulation; late embryonic losses (%): percentage of mares that lost their Day 16 pregnancies between Days 16 and 39 post-ovulation; early fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 40 and 90 post-ovulation; mid-fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 91 and 198 post-ovulation; late fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 199 and live foaling; overall embryonic mortality (EM) plus FF (%): percentage of mares that were detected non-pregnant on Day 39 post-ovulation; overall fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
244
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
Table 2 Effects of reproductive status on measures of reproductive efficiency in Thoroughbred mares. Reproductive parameters
Reproductive status Foaling (n = 713)
Barren (n = 155)
Maiden (n = 101)
Rested (n = 62)
Aborted (n = 85)
Repeated (n = 50)
Management of estrus No. oestrous cycles No. matings per oestrus (S.D.) No. matings per Day 16 conception (S.D.)
1156 1.45 (0.44) 2.74 (0.61)
287 1.44 (0.73) 3.27 (0.68)
169 1.49 (0.88) 2.71 (1.04)
115 1.45 (0.91) 3.48 (0.68)
167 1.46 (0.78) 3.20 (0.83)
82 1.50 (0.82) 3.24 (0.88)
Pregnancy results Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Day 16 pregnancies per season (%) Un-detected EEM plus FF (%) Late embryonic losses (%) Early fetal losses (%) Mid-fetal losses (%) Late fetal losses (%) Overall EM plus FF (%) Overall fetal losses (%) Overall detected pregnancy losses (%) Mares did not produce a foal (%) Mares produced a live foal (%)
53.03 48.53ac 44.46a 85.97 14.03 8.48 2.61 2.77a 2.28 21.32 7.67a 16.15a 27.91ac 72.09ac
43.90 37.63b 33.80b 81.29 18.71 14.29 1.59 4.76 2.38 30.32a 8.73 23.02 37.42 62.58
55.03 52.66c 46.75 92.08 7.92 4.30 4.30 4.30 2.15 11.88b 10.75 15.05 21.78a 78.22a
41.74 34.78ab 30.43 77.42 22.58 16.67 4.17 6.25 0.00 35.48a 10.42 27.08 43.55c 56.45c
45.51 40.12 31.74b 89.41 10.59 11.84 3.95 11.84b 2.63 21.18 18.42b 30.26b 37.65 62.35
46.34 37.80 31.71 76.00 24.00 18.42 2.63 5.26 5.26 38.00a 13.16 31.58 48.00b 52.00b
Values in the same row with different letters (a–c) or lacking a common letter differ significantly: Bonferroni (P < 0.003); S.D. (standard deviation). Day 16 pregnancies per season (%): percentage of mares detected pregnant on day 16 post-ovulation during the season; un-detected early embryonic mortality (EEM) plus fertilization failure (FF) (%): percentage of mares that were detected non-pregnant on Day 16 post-ovulation; late embryonic losses (%): percentage of mares that lost their Day 16 pregnancies between Days 16 and 39 post-ovulation; early fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 40 and 90 post-ovulation; mid-fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 91 and 198 post-ovulation; late fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 199 and live foaling; overall embryonic mortality (EM) plus FF (%): percentage of mares that were detected non-pregnant on Day 39 post-ovulation; overall fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
associated with spontaneous ovulation (Table 3). However, the number of matings per oestrus and matings per Day 16 pregnancy were significantly reduced when ovulation was induced hormonally (P < 0.001). 3.2. Pregnancy losses Overall 31.05% of the total mares failed to produce a foal and a major proportion of these were contributed by unobserved EEM plus FF (Table 1). Collectively, the overall EM plus FF accounted for 75% of mares that did not produce
a foal. The overall percent fetal and observed pregnancy losses were found to be 9.26% and 19.11%, respectively. Further, the late embryonic mortality (observed between Days 16 and 39) constituted more than 50% of the overall detected pregnancy losses (Table 1). When the chronic aborters and chronic barren mares were excluded from the analysis, overall percent EM plus FF occurred between Days 0 and 39 was analyzed as 18.80%, whereas overall percent detected pregnancy losses were found to be 15.27%. The incidence of percent undetected EEM plus FF was much higher (P < 0.0001) in mares age ≥18 years than
Table 3 Effects of hormonal induction of ovulation on reproductive parameters in 253 Thoroughbred mares surveyed over a period of 7 years. Reproductive parameters
No. oestrous cycles (% of total) No. matings (% of total) No. 16-day pregnancies (% of total) No. matings per oestrus ± S.D. No. matings per Day 16 pregnancy ± S.D. Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Late embryonic losses (%) Overall Fetal losses (%) Overall detected pregnancy losses (%) Detected pregnancies produced a live foal (%)
Type of ovulation Induced
Spontaneous
370 (18.72) 464 (16.13) 202 (20.32) 1.25a ± 0.49 2.30a ± 0.53 54.59 49.46 45.95 9.41 6.43 15.84 84.16
1606 (81.28) 2412 (83.87) 792 (79.68) 1.50b ± 0.74 3.05b ± 0.75 49.32 44.40 39.48 9.97 9.97 19.95 80.05
Values in the same row with different letter (a and b) are significantly different: Bonferroni (P < 0.001); S.D. (standard deviation). Overall fetal losses (%): percentage of mares that lost their pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
BL
20 (40.00) 30 (60.00) 18.66 ± 2.84 15 29 41 (87.23) UL UL
4 (28.57)
Both Single
BL
Manual crushing
UL
Spontaneous/simultaneous reduction of conceptuses
BL
Prostaglandin termination
UL
3–7 and 8–12 years old mares. Furthermore, the overall percent EM plus FF were significantly lower in mares at ages 3–7 years (16.38%) and 8–12 years (21.53%) than ≥18 years old (54.55%). Mares aged ≥18 years demonstrated the greater (P < 0.001) percent late embryonic losses than 3–7- and 8–12-year age groups. Although, no differences were observed in overall fetal losses, but the percentage of mid-fetal losses (20.00%) and overall percent detected pregnancy losses (46.43%) were much higher in ≥18 years old mares compared to other age groups (P < 0.008; Table 1). Regarding mare status, undetected EEM plus FF and percent late embryonic losses were similar (P > 0.003) across all the groups. The overall percent EM plus FF was lower in maiden mares (11.88%; P < 0.001) than repeated (38.00%), rested (35.48%) and barren (30.32%) mares. Aborted mares showed higher percent mid-fetal as well as overall percent fetal and detected pregnancy losses than foaling mares (P < 0.003; Table 2). Further, greater proportion of repeated (48.00%) and rested (43.55%) mares did not produce a foal compared to maiden mares (21.78%; P < 0.003). No significant differences in terms of percent overall detected pregnancy losses and fetal losses were observed with the number of matings per oestrus, induced/spontaneous oestrus and ovulation, stud farm surveyed, and month of mating or the breeding year.
245 6 (50.00) 6 (50.00) 24.51 ± 1.98 0 0 (0)
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
BL
1 (7.14) 19.42 ± 3.17 0 0 (0) 9 (64.29) 26 (86.67) 4 (13.33) 21.15 ± 3.10 24 3 26 (86.67)
Outcome
Type of fixation: UL: unilateral; BL: bilateral; UTB: uterine body.
A total of 108 multiple pregnancies (106 twins and 2 triplets) were recorded in the study with an overall incidence of 5.40% of the total mated oestrus (10.70% of the total pregnancies; 9.14% of mare years). Amongst the twin pregnancies, 61 (57.57%) were unilateral, 44 (41.50%) were bilateral and 1 case was fixed in uterine body. The fate of multiple pregnancies is given in Table 4. The percent late embryonic losses in twin pregnancies were higher (P = 0.0016) than the overall singleton pregnancies (21.98% vs. 8.64%, respectively). There was a 15% increase in the success rate of manual crushing when two concepti were
Number of twins (percentage) Mean day of diagnosis/intervention ± S.D. No. Day 39 pregnancies No. foaling (percentage)
3.4. Multiple pregnancies
Table 4 Outcome of twin pregnancies in 253 Thoroughbred mares over a period of 7 years.
The overall live foaling rate was 68.95%. Foaling rates were higher (P < 0.0001) for mares aged 3–7 years (76.55%) than for mares at ages 13–17 years (61.99) and ≥18 years (34.09%; Table 1). Similarly, mares at ages 3–7 and 8–12 years showed more foaling per oestrus than ≥18-year olds (Table 1). When compared by reproductive status, foaling rates were significantly lower in repeated (52.00%) mares than foaling (72.09%) and maiden (78.22%) mares (Table 2). Further, significantly more foaling rates were observed in maiden than rested mares (P < 0.003). The percent foaling per oestrus was significantly higher in foaling mares compared to barren and aborted mares (P < 0.003; Table 2). The percent foaling per oestrus did not differ significantly in mares covered for ≤2 oestrous cycles (41.82%) than in mares covered during ≥3 oestrous cycles (32.19%) per breeding season. Further, the number of matings per oestrus, type of oestrus, month of mating, stud farm and year did not affect the foaling rates (P > 0.05).
UTB
3.3. Foaling rates
246
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
distributed bilaterally. Both sets of triplet pregnancies were treated successfully by crushing two concepti on the same day. 4. Discussion To the best of our knowledge, this is the first extensive report on reproductive efficiency of Thoroughbred mares of subtropical environment from Indian subcontinent that takes into consideration the effect of age and prior reproductive history on various reproductive parameters. The overall Day 16 per cycle pregnancy rate observed (50.30%) in the present study is lower than the range (54–64%) previously reported for Thoroughbred mares from the temperate regions of world (Brück et al., 1993; Hemberg et al., 2004; Allen et al., 2007). Similarly, the foaling rates are comparatively lower than several studies, but the overall per cycle pregnancy loss rates are only slightly lower than many recent studies (Brück et al., 1993; Morris and Allen, 2002). The more frequent use of diagnostic ultrasonography at the stud farms mentioned in the reports compared with our study (with only 3/4th got scanned), somewhat explains the origin of difference in the pregnancy rates. The use of ultrasonographic examination facilitates an early diagnosis of pregnancy as well as an accurate diagnosis of uteroovarian pathologies that affect the mare fertility, which consequently alters the pregnancy rates at different days (Noakes, 2001). The identification of age as a major factor influencing the pregnancy rates in Thoroughbred mares is in agreement with several other studies (Davies Morel et al., 2005; Allen et al., 2007). The decline in fertility with age has been attributed to chronic progressive degenerative changes in the endometrium (Ricketts and Alonso, 1991) along with potential susceptibility to uterine infection arising from poor perineal conformation and uterine incompetence that is observed with senescence (Kalirajan and Rajasundaram, 2008). Our study also supported a previous finding (Morris and Allen, 2002) that resting a mare may not be advantageous to get her pregnant in the next season as higher Day 39 pregnancy rates were observed in maiden mares as compared to rested mares of the present survey. However, the effect of mare’s reproductive status on pregnancy rates is still a controversial issue as some recent studies (Hemberg et al., 2004; Allen et al., 2007) in Thoroughbred mares are supportive, while findings of Brück et al. (1993) are contradictory to our observations. It is worth noting that the bigger proportion of comparatively older (13 years) mares fell in barren (40.65%) category, whereas all of the maiden mares and 3/4th of the foaling mares were less than 13 years of age. This might be responsible for the differences in the pregnancy rates with regard to reproductive status. About 50% of the mares that did not successfully foal for two seasons failed to do so in the next seasons as well, thus culling these mares might improve overall reproductive performance of the stud farm. The observed mean number of matings/oestrus and matings per pregnancy is relatively higher than the recent surveys from other countries (Allen et al., 2007). Perhaps it reflects a difference in reproductive management for predicting the optimal time of breeding and greater will-
ingness to rebred mares that fail to ovulate 36–48 h after previous matings. Our results are in agreement with the previous studies (Davies Morel and Gunnarsson, 2000; Morris and Allen, 2002) where no effect of number of matings or inseminations on pregnancy rates was observed. A decrease in Day 16 pregnancy rate with increase in number of covered oestrous cycles reported previously by Brück et al. (1993) was not seen in our study. The use of exogenous hormones to induce ovulation had no benefit over spontaneous ovulations in terms of per cycle pregnancy rates, as also reported by Morris and Allen (2002) and Davies Morel and Newcombe (2008). However, as evident from this and other studies (Grimmett and Perkins, 2001; Allen et al., 2007) hormonal induction of ovulation reduces the number of matings per oestrus and matings required per pregnancy. This might be due to increased ovulation rate with in 48 h of administration (98%) (Camillo et al., 2004) and therefore serves as an important tool to deal adequately with the markedly increased number of mares booked to popular stallions. The Day 16 pregnancy rates did not show a significant change over different months of the breeding seasons. Therefore, we were not able to demonstrate a significant decline in reproductive performance despite a rise in temperature (35–45 ◦ C) coinciding with peak breeding period (mid-April) of Thoroughbred mares in northwestern India. Similarly, Mortensen et al. (2009) obtained an acceptable embryo recovery rates (63%) from non-exercised mares during the warmest period (>30 ◦ C) of the year in central Texas. Although, estimating fertilization rate is a prerequisite to determine the exact magnitude of EEM, but it is impractical to differentiate between undetected EEM and FF under field conditions. It is generally accepted that fertilization rate in mares is generally over 90%, and is independent of age and mares status (Ball et al., 1989). In addition, the chances of fertilization failures were further lower in our study as most of the mares were covered for more than one oestrus in a season. It is likely, therefore, that the EEM is the major causative factor for subfertility in the mares, which were detected as non-pregnant on Day 16 post-ovulation. It might be possible that most of the undetected EEM occurs due to failure of maternal recognition of pregnancy during first 16 days of gestation in mares (Roberts et al., 1996) and extent of it still needs to be ascertained. The percent late embryonic mortality observed in the current survey fell within the previously reported range (5–18%) for Thoroughbreds (Simpson et al., 1982; Malschitzky et al., 2003). A major proportion (∼75%) of pregnancy failures and losses occurred before Day 40, as reported elsewhere (Morris and Allen, 2002; Yang and Cho, 2007). The issue of increase in percent late embryonic as well as overall detected pregnancy losses and decrease in pregnancy rates with advancing age (Carnevale and Ginther, 1992) are intermingled. In addition to factors discussed earlier, older mares have more incidences of multiple uterine cysts causing reduction in uterine vascular perfusion (Ferreira et al., 2008) along with frequent delayed and irregular ovulations (Carnevale et al., 1994) that release morphologically/genetically abnormal oocytes (Carnevale et al., 1999; Rambags et al., 2005) and renders
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
them subfertile. The increase in age did not affect incidence of overall percent fetal losses as shown earlier (Brück et al., 1993). However, significant differences were observed in percent mid-fetal losses that might be associated with poor placental efficiency and compromised microplacentomes devolvement in subfertile older mares (Bracher et al., 1996; Abd-Elnaeim et al., 2006) during this period. As aborted mares lost their fetus more frequently, it indicates the need of careful management in these mares. Furthermore, it is evident in the current investigation that repeated mares experienced similar pregnancy rates as well as percent embryonic, fetal and overall pregnancy losses than other reproductive statuses. It reflects the potential success of rebreeding mares in same season after experiencing a late embryonic mortality. Hence, it is advisable to breed a mare in the same season as this may have implication for stud management where the expectation is that broodmares will produce a live foal each year. With respect to twining, the overall per cycle twin pregnancy rate was well in the range of 2.1–16.2% reported across the world (Sanderson and Allen, 1987; Newcombe, 1995). As we found a lesser use (18.72%) of exogenous use of hormones than in Thoroughbred stud farms of other (59.10%) counties like United Kingdom (Allen et al., 2007), our study does not support the work of Veronesi et al. (2003) that associated the rise in twining with more increase use of hormones. Similar to previous report (Ginther, 1989a), there were more chances of unilateral fixation of twins that will get spontaneously reduced to a singleton most likely between Days 17 and 30 of pregnancy (Ginther, 1989b; Brück et al., 1993). The percent late embryonic losses of 21.98% confirmed the previous findings (Brück et al., 1993; Yang and Cho, 2007) of greater late embryonic losses in twins than for singleton pregnancy. The success rate of manual compression was 87.04% and is comparable to various reports (Merkt and Jöchle, 1993; Hemberg et al., 2004). However, we did not observe a difference between the percent late embryonic and fetal losses in both spontaneously reduced and manually crushed twin pregnancies, which is in contrast to reported increase in fetal losses after manual crushing (Brück et al., 1993). The 15% difference of bicornuate compared to unicornuate success rate of ‘pinching’ may be explained by increased ease of manipulation and/or reduced risk of damaging the neighboring conceptus. The high success of manually reducing twins to singleton may consequently increase the overall reproduction indices as such pregnancies have a chance to terminate with birth of a sound and well-developed foal (Ricketts and Young, 1990; Górecka and Jezierski, 2003). Besides the factors discussed above, other confounding variables that may affect the reproductive performance of mares are stallion’s fertility, nutrition and management of stud farms. So far, the studies on stallion fertility (Davies Morel and Gunnarsson, 2000; Morris and Allen, 2002) have been inconclusive over its effects on fertility rates. While, a long term restricted nutrition may lower mare fertility (Niekerk van and Niekerk van, 1998; Henneke et al., 1984). However, in our study any nutritional effect on reproductive performance would have been minimal as the data was collected from well-organized Thoroughbred stud
247
farm where as a standard practice the nutrition is, though not specified, considered to be good. Both of the above mentioned factors were not analyzed in this study since they can be thoroughly investigated in a controlled study only. 5. Conclusion In summary, no effect of summer stress on fertility of mares was evident, therefore a comparatively lower reproductive performance of Thoroughbreds mares bred under Indian subtropical conditions than mares of temperate regions might be due to the differences in breeding management. Further, mare age and her reproductive status strongly influenced the reproductive efficiency. In order to improve the overall reproductive performance of a stud farm, it is advisable to rebreed the mare that had lost its earlier pregnancy in the same season, and cull the chronic barren and habitual aborter mares. Acknowledgements The authors are grateful to the veterinarians, owners, staff and management of the surveyed stud farms, for access to their records and help with extraction of relevant information. Dr. G.V.P. Ravi Kumar, Assistant Professor, Department of Animal Breeding and Genetics, GADVASU, Ludhiana, Punjab, India is acknowledged for helping with statistical analysis. References Abd-Elnaeim, M.M.M., Leiser, R., Wilsher, S., Allen, W.R., 2006. Structural and haemovascular aspects of placental growth throughout gestation in young and aged mares. Placenta 27, 1103–1113. Allen, W.R., Brown, L., Wright, M., Wilsher, S., 2007. Reproductive efficiency of Flatrace and National Hunt Thoroughbred mares and stallions in England. Eq. Vet. J. 39, 438–445. Ball, B.A., Little, T.V., Hillman, R.B., Woods, G.L., 1989. Survival of Day 4 embryos from young, normal mares and aged, sub fertile mares after transfer to normal recipient mares. J. Reprod. Fertil. 85, 187–194. Bracher, V., Mathias, S., Allen, W.R., 1996. Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Eq. Vet. J. 28, 180–188. Brück, I., Anderson, G.A., Hyland, J.H., 1993. Reproductive performance of Thoroughbred mares on six commercial stud farms. Aust. Vet. J. 70, 299–303. Camillo, F., Pacini, M., Panzani, D., Vannozzi, I., Rota, Al, Aria, G., 2004. Clinical use of twice daily injections of buserelin acetate to induce ovulation in the mare. Vet. Res. Commun. 28, 169–172. Carnevale, E.M., Ginther, O.J., 1992. Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology 37, 1101–1115. Carnevale, E.M., Bergfelt, D.R., Ginther, O.J., 1994. Follicular activity and concentrations of FSH and LH associated with senescence in mares. Anim. Reprod. Sci. 35, 231–246. Carnevale, E.M., Uson, M., Bozzola, J.J., King, S.S., Schmitt, S.J., Gates, H.D., 1999. Comparison of oocytes from young and old mares with light and electron microscopy. Theriogenology 51, 299. Davies Morel, M.C.G., Gunnarsson, V., 2000. A survey of the fertility of Icelandic stallions. Anim. Reprod. Sci. 64, 49–64. Davies Morel, M.C.G., Newcombe, J.R., 2008. The efficacy of different hCG dose rates and the effect of hCG treatment on ovarian activity: ovulation, multiple ovulation, pregnancy, multiple pregnancy, synchrony of multiple ovulation; in the mare. Anim. Reprod. Sci. 109, 189–199. Davies Morel, M.C.G., Newcombe, J.R., Swindlehurst, J.C., 2005. The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare. Theriogenology 63, 2482–2493. Engelken, T.J., 1999. Reproductive health programs for beef herds: analysis of records for assessment of reproductive performance. In:
248
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
Youngquist, R.S. (Ed.), Current Therapy in Large Animal Theriogenology. W.B. Saunders Co., Philadelphia, pp. 451–456. Ferreira, J.C., Gastal, E.L., Ginther, O.J., 2008. Uterine blood flow and perfusion in mares with uterine cysts: effect of the size of the cystic area and age. Reproduction 135, 541–550. Ginther, O.J., 1989a. Twin embryos in mares. I. From ovulation to fixation. Eq. Vet. J. 21, 166–170. Ginther, O.J., 1989b. Twin embryos in mares. II. Post fixation embryo reduction. Eq. Vet. J. 21, 171–174. Ginther, O.J., Gastal, E.L., Gastal, M.O., Beg, M.A., 2004. Seasonal influence on equine follicle dynamics. Anim. Reprod. 1, 31–44. Górecka, A., Jezierski, T., 2003. Effect of single vs multiple ovulations on oestrus behavior and pregnancy rate in Thoroughbred mares. Animal Science Papers and Reports, vol. 21. Institute of Genetics and Animal ˛ Breeding, Jastrzebiec, Poland, pp. 27–33. Grimmett, J.B., Perkins, N.R., 2001. Pregnancy and twinning rates in Thoroughbred mares following the administration of human chorionic gonadotrophin (hCG). N. Z. Vet. J. 49, 94–100. Hemberg, E., Lundeheim, N., Einarsson, S., 2004. Reproductive performance of Thoroughbred mares in Sweden. Reprod. Domest. Anim. 39, 81–85. Henneke, D.R., Potter, G.D., Kreider, J.L., 1984. Body condition during pregnancy and lactation and reproductive efficiency in mares. Theriogenology 21, 256–258. Ju, J.C., Tseng, J.K., 2004. Nuclear and cytoskeleton alterations of in vitro matured porcine oocytes under hyperthermia. Mol. Reprod. Dev. 68, 125–133. Kalirajan, R., Rajasundaram, R.C., 2008. Incidence of endometritis in relation to age and Caslick index in mares. Indian Vet. J. 85, 893–894. Kranzler, G., Moursund, J., 1999. Statistics for the Terrified, 2nd ed. Prentice Hall, Upper Saddle River, pp. 120–125. Malschitzky, E., Schilela, A., Mattos, A.L.G., Garbade, P., Gregory, R.M., Mattos, R.C., 2003. Intrauterine fluid accumulation during foal heat increases embryonic death. Pferdeheilkunde 19, 246–249. Marai, I.F.M., El-Darawany, A.A., Fadiel, A., Abdel-Hafez, M.A.M., 2007. Physiological traits as affected by heat stress in sheep—a review. Small. Rumin Res. 71, 1–12. Merkt, H., Jöchle, W., 1993. Abortions and twin pregnancies in Thoroughbreds: rate of occurrence, treatments and prevention. J. Eq. Vet. Sci. 13, 690–694. Morris, L.H.A., Allen, W.R., 2002. Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket. Eq. Vet. J. 34, 51–60.
Mortensen, C.J., Choi, Y.H., Hinrichs, K., Ing, N.H., Kraemer, D.C., Vogelsang, S.G., Vogelsang, M.M., 2009. Embryo recovery from exercised mares. Anim. Reprod. Sci. 110, 237–244. Nagamine, Y., Sasaki, O., 2008. Effect of environmental factors on fertility of Holstein–Frisian cattle in Japan. Livest. Sci. 115, 89–93. Newcombe, J.R., 1995. Incidence of multiple ovulations and multiple pregnancies in mares. Vet. Rec. 137, 121–123. Niekerk van, F.E., Niekerk van, C.H., 1998. The effect of dietary protein on reproduction in the mare. VII. Embryonic development, early embryonic death, foetal losses and their relationship with serum progestagen. J. S. Afric. Vet. Assoc. 69, 150–155. Noakes, D., 2001. Pregnancy and its diagnosis. In: Noakes, D.E., Parkinson, T.J., England, G.C.W. (Eds.), Arthtur’s Veterinary Reproduction and Obstetrics. W.B. Saunders Company, Philadelphia, pp. 69–118. Rambags, B.P., Krijtenburg, P.J., Drie, H.F., Lazzari, G., Galli, C., Pearson, P.L., Colenbrander, B., Stout, T.A., 2005. Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87. Ricketts, S.W., Young, A., 1990. Thoroughbred mare fertility. Vet. Rec. 128, 68. Ricketts, S.W., Alonso, S., 1991. The effect of age and parity on the development of equine chronic endometrial disease. Eq. Vet. J. 23, 189–192. Roberts, R.M., Xie, S., Mathialagan, N., 1996. Maternal recognition of pregnancy. Biol. Reprod. 54, 294–302. Sanderson, M., Allen, W.R., 1987. Reproductive efficiency of Thoroughbred mares in the UK. In: Proceedings of the 9th Bain-Fallon Memorial Lectures. Australian Equine Veterinary Association, Sydney, Australia, pp. 31–41. Schulman, M.L., Marlow, C.H., Nurton, J.P., 2003. A survey of reproductive success in South African Thoroghbred horse breeding from 1975 to 1999. J. S. Afric. Vet. Assoc. 74, 17–19. Simpson, D.J., Greenwood, R.E., Ricketts, S.W., Rossdale, P.D., Sanderson, M., Allen, W.R., 1982. Use of ultrasound echography for early diagnosis of single and twin pregnancy in the mare. J. Reprod. Fertil. Suppl. 32, 431–439. Veronesi, M.C., Battocchio, M., Faustini, M., Gandini, M., Cairolia, F., 2003. Relationship between pharmacological induction of estrous and/or ovulation and twin pregnancy in the Thoroughbred mares. Domest. Anim. Endocrinol. 25, 133–140. Yang, Y.J., Cho, G.J., 2007. Factors concerning early embryonic death in Thoroughbred mares in South Korea. J. Vet. Med. Sci. 69, 787–792.
Contents lists available at ScienceDirect
Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Reproductive efficiency of Thoroughbred mares under Indian subtropical conditions: A retrospective survey over 7 years夽 Sumeet Sharma a,∗ , G.S. Dhaliwal b , Dinesh Dadarwal c,1 a
Civil Veterinary Hospital, Mahatam Nagar, Fazilka, Punjab 152 123, India Department of Veterinary Clinical Services Complex, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, Punjab 141004, India c Department of Animal Reproduction, Gyanecology and Obstetrics, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana, Punjab 141004, India b
a r t i c l e
i n f o
Article history: Received 18 September 2008 Received in revised form 4 May 2009 Accepted 14 May 2009 Available online 21 May 2009 Keywords: Mare Reproductive efficiency Pregnancy loss Summer stress Embryonic mortality
a b s t r a c t Service records of 253 mares (1181 mare-years) spanning over 7 consecutive years, from nine organized Thoroughbred stud farms, situated in the subtropical northwestern India were retrospectively analyzed to assess their reproductive performance. The overall per cycle pregnancy rate at Day 16 and overall foaling rates were 50.30% and 68.95%, respectively, and were significantly higher in mares aged 3–7 years than ≥18 years old mares. The late embryonic losses (9.86%) that occurred between Days 16 and 39 post-ovulation contributed more than 50% of the overall detected pregnancy losses (19.11%). The overall percent detected pregnancy losses were lower in mares at ages 3–7 years compared to those at ages ≥18 years (14.78% vs. 46.43%, respectively; P < 0.0001). Chronic barren and habitual aborter mares tended to affect reproductive efficiency of mares. Fifty percent of the mares that experienced ≥2 consecutive abortions or barren years, again stayed aborted or barren in the next seasons, respectively. No effect of numbers of matings per oestrus was observed on overall fertility. Neither the induction of oestrus nor ovulation by exogenous hormonal treatment had any effect on most of the analyzed reproductive parameters. Regarding breeding month or years, the reproductive efficiency did not differ significantly. The incidence of multiple pregnancies was 5.40% and percent late embryonic loses were higher (P = 0.0016) in twin (21.98%) than singleton (8.64%) pregnancies. In conclusion, comparatively lower fertility rates were recorded in Thoroughbred mares bred under Indian subtropical climatic conditions than those reported from temperate regions that might be due to difference in breeding management rather than prevailing environment. © 2009 Elsevier B.V. All rights reserved.
1. Introduction
夽 The present study is a part of the MVSc thesis submitted by the first author to the Department of ARGO, Punjab Agricultural University, Ludhiana, India. ∗ Corresponding author at: Street No. 3, Shakti Nagar, Fazilka, Punjab 152 123, India. Tel.: +91 1638 263330. E-mail address: [email protected] (S. Sharma). 1 Present address: Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, 52 Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, S7N 5B4, Canada. 0378-4320/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2009.05.011
Mares have the lowest fertility rate compared to females of other domesticated species, as horse breeds have been selected based on war, draft and racing abilities rather than fertility (Engelken, 1999). Further, in Thoroughbred horses, pedigree and track records are the highest priority for selecting the best of the breed, and generally overlooks the physiological and managerial factors that might affect reproductive performance during their breeding career. Over the last two decades, retrospective studies on fertility in Thoroughbred mares across the world have revealed per cycle pregnancy rates ranging from 54% to 64% (Brück et
242
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
al., 1993; Allen et al., 2007), while, the cumulative end-ofseason pregnancy rates and foaling rates ranged from 85% to 95% (Morris and Allen, 2002; Hemberg et al., 2004) and 62–83% (Morris and Allen, 2002; Schulman et al., 2003), respectively. For the Thoroughbred mares in northern hemisphere, a 4-month breeding period (February–June) is arbitrarily imposed for the purpose of age-related racing. In northwestern India, mares experience high ambient temperature and increased relative humidity for almost half of the breeding period (mid-April to mid-June). The deleterious effects of summer stress on fertility have been well documented in other farm species (Ju and Tseng, 2004; Marai et al., 2007; Nagamine and Sasaki, 2008). However, no such information in Thoroughbred mares exists to the best of our knowledge. Moreover, in an evolutionary perspective, horses prefer temperate climate (Ginther et al., 2004) and the effect of change of climate on their reproductive performance have not been critically investigated. Thus, we investigated reproductive performance of Thoroughbred mares bred under Indian subtropical conditions. A thorough understanding of factors influencing reproductive efficiency should help to identify mares at greatest risk of pregnancy loss and also to organize breeding management in a way best suited to obtain optimal fertility. 2. Materials and methods 2.1. Database Service records of 253 mares for seven consecutive (1998–2005) breeding seasons (February–June) from nine organized Thoroughbred stud farms of northwestern India (lies between 28◦ 28 and 30◦ 30 N latitude and between 74◦ 31 and 77◦ 02 E longitude) were analyzed. A survey form was prepared and fertility data for the mares was recorded. As the records of the stud farms were confidential, all the stud farms and mares were identified by numerical codes only. 2.2. Groups The mares were grouped according to age (3–7, 8–12, 13–17, ≥18 years), reproductive status, i.e. maiden (never mated), barren (mated without a pregnancy at the end of last breeding season), foaling (foaled in the current season and lactating throughout the season), rested (parous mare deliberately not mated during the last breeding season), aborted (pregnant at the end of last breeding season but lost pregnancy later on and/or did not foal) and repeated (mares rebred again in the same season after losing a detected pregnancy irrespective of previous status and considered as a new mare year). 2.3. Management On all stud farms included in the survey, mares were fed a daily ration according to their reproductive status in a manner that is generally practiced in India
(Lucerne/hay and paddock grass ad libitum plus approximately 5 kg of concentrate divided twice or thrice in a day). Oestrus was monitored daily by teasing, and ultrasonographic/transrectal examination was carried out daily or every other day to follow the dominant follicular development and to confirm ovulation. All the mares were checked by the veterinarian for the follicle size and consistency and thereafter mated with a stallion of acceptable fertility. Mares were mated again at 36–48 h later if the follicle was still present at second examination. In small proportion of mares in which either the ovulation was not monitored after covering or record was unavailable, the day following last mating was assumed as day of ovulation (Day 0). Pregnancy diagnosis was first performed on an average Day 16 post-ovulation, by ultrasonography and/or transrectal palpation and subsequently, on an average Days 21, 32, 39, 50, 65, 90, 135 and 198 postovulation. 2.4. Records The data recorded on the survey forms was analyzed retrospectively after the incomplete individual records had been omitted. Since most of the mares returned to the same stud farm for several years and were bred for more than one breeding season, the terms ‘mare’ and ‘mare-year’ are used synonymously in the rest of the article. Although, original data included 1181 mare-years, but fertility analysis was carried out on 1166 mares after excluding mares that had both of their twin concepti reduced after manual intervention. The reduction with manual intervention by compression was considered successful if the twins were reduced to singleton when examined 3 days later. The pregnancy rates were calculated based on per oestrous cycle (per cycle pregnancy rate Day 16/Day 39) and per season (percentage of mares detected pregnant on Day 16 post-ovulation during the season). However, per cycle pregnancy rate at Day 16 was used for further calculations, it is being synonymously used with Day 16 pregnancy rates. The analyzed pregnancy losses included late embryonic losses occurred between Days 16 and 39, fetal losses from Day 40 post-ovulation to term (early fetal losses—Days 40–90; mid-fetal losses—Days 91–198; late fetal losses—Day 199 to foaling) and overall detected pregnancy losses occurred between Day 16 and foaling. The terms, percent ‘undetected early embryonic mortality (EEM) plus fertilization failure (FF)’ and ‘overall embryonic mortality (EM) plus FF’, were used for the percentage of mares that were detected non-pregnant at Days 16 and 39 post-ovulation, respectively. 2.5. Statistical analysis Statistical analyses were preformed on subpopulation of all the mares with complete information from mating to foaling, about their age, reproductive status, etc. using statistical software Minitab 14 version (Minitab Inc., USA). Chi-squared tests were used to determine if there was an overall effect of each variable on the outcome of interest (Kranzler and Moursund, 1999). If this effect of variable(s) was significant (P < 0.05), multiple
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
243
39 pregnancy rates were recorded in maiden than rested (34.78%) mares. However, the Day 16 pregnancy rates per season were not influenced by the reproductive status of mares (Table 2). Day 16 pregnancy rates in mares that were covered for ≤2 oestrous cycles and ≥3 oestrous cycles in a breeding season were 51.11% and 44.21%, respectively, and the difference was not significant under Bonferroni adjustment. Also, stud farm surveyed, the month and year in which mating occurred had no effect on Day 16 pregnancy rates. Of the total number of mated oestruses, 1597 (80.82%) occurred spontaneously and remaining 379 (19.18%) were induced by treatment with one or combination of frequently used exogenous hormone preparation namely: (i) prostaglandin F2␣ or its natural or synthetic analogues (cloprostenol, dinoprost tromethamine) given IM; (ii) 10 days after withdrawal of orally active progestagen, allyl trenabolone (Regumate® ; Intervet India, Pune, India). There was no significant difference in Day 16 pregnancy rate from matings at spontaneous (49.84%) vs. hormone-induced (52.24%) oestrus. The ovulation occurred spontaneously in 81.28% of reported oestrous periods, while, human chorionic gonadotrophin (hCG; Chorulon® , IV; Intervet India, Pune, India), cloprostenol/dinoprost (Estrumate® IM; Schering Plough Animal Health, NJ, USA;/Lutalyse® IM; Pfizer India Limited, Mumbai, India) and buserelin (Receptal® , IV; Intervet, Pune, India) were administered in 17%, 1% and 0.7% of oestrous periods, respectively, to induce ovulation. Inducing ovulation with exogenously administered hormones had no effect upon Day 16 pregnancy rate compared to that
comparisons were carried out and each comparison was considered significant only after making the Bonferroni adjustment. 3. Results 3.1. Management of the oestrous cycle and pregnancy rates The population distribution of mares on the basis of their age and reproductive status are shown in Tables 1 and 2. A sum total of 1166 mares were mated once or more times during 1976 oestrous periods to give an overall per cycle pregnancy rate at Day 16 of 50.30%, while, overall per cycle pregnancy rate at Day 39 was 45.34%. By the end of the season 994 (85.25%) mares had been diagnosed pregnant at around Day 16 post-ovulation. There were 8 aborters and 11 barren mares, which stayed aborters or barrens, respectively, for at least 2 consecutive years with maximum of four breeding seasons. On excluding these mares, the remaining 1053 mare years (1732 oestruses), had overall Day 16 per cycle pregnancy rate of 53.70%. Age of mare markedly affected both per cycle pregnancy rates at Day 16 and Day 16 pregnancy rates per season, as mares at ages 3–7 and 8–12 years had significantly higher rates than ≥18 years old mares (Table 1). Although, reproductive status of mare did not influence Day 16 pregnancy rates under Bonferroni adjustment at P < 0.003 (Table 2), but, Day 39 pregnancy rates were higher (P < 0.003) in maiden (52.66%) and foaling mares (48.53%) compared to barren mares (37.63%). Additionally, greater (P < 0.003) Day Table 1 Effects of age on measures of reproductive efficiency in Thoroughbred mares. Reproductive parameters
Mare age (years)
Mean (n = 1166)
3–7 (n = 354)
8–12 (n = 497)
13–17 (n = 271)
≥18 (n = 44)
Management of estrus Number of oestrus cycles Number of matings per oestrus (S.D.) Number of matings per Day 16 conception (S.D.)
588 1.50 (0.74) 2.77 (0.67)
830 1.44 (0.65) 2.77 (0.68)
480 1.43 (0.71) 3.16 (0.75)
78 1.47 (0.81) 4.11 (0.93)
1976 1.46 (0.71) 2.89 (0.79)
Pregnancy results Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Day 16 pregnancies per season (%) Un-detected EEM plus FF (%) Late embryonic losses (%) Early fetal losses (%) Mid-fetal losses (%) Late fetal losses (%) Overall EM plus FF (%) Overall fetal losses (%) Overall detected pregnancy losses (%) Mares did not produce a foal (%) Mares produced a live foal (%)
54.08a 50.34a 46.09a 89.83a 10.17a 6.92 a 2.70 3.47a 2.52 16.38a 7.86 14.78a 23.45a 76.55a
51.93ab 46.99ab 42.17ab 86.72ab 13.28ab 9.51a 3.33 4.24a 3.05 21.53ab 9.28 18.79a 29.58ab 70.42ab
45.21bc 39.58b 35.00b 80.07bc 19.93bc 12.44 3.68 6.01 2.33 29.89b 10.14 22.58a 38.01b 61.99b
35.90c 25.64c 19.23c 63.64c 36.36c 28.57b 0.00 20.00b 6.25 54.55c 17.86 46.43b 65.91c 34.09c
50.30 45.34 40.69 85.25 14.75 9.86 3.13 4.72 2.78 23.16 9.26 19.11 31.05 68.95
Values in the same row with different letters (a–c) or lacking a common letter differ significantly: Bonferroni (P < 0.008); S.D. (standard deviation). Day 16 pregnancies per season (%): percentage of mares detected pregnant on day 16 post-ovulation during the season; un-detected early embryonic mortality (EEM) plus fertilization failure (FF) (%): percentage of mares that were detected non-pregnant on Day 16 post-ovulation; late embryonic losses (%): percentage of mares that lost their Day 16 pregnancies between Days 16 and 39 post-ovulation; early fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 40 and 90 post-ovulation; mid-fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 91 and 198 post-ovulation; late fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 199 and live foaling; overall embryonic mortality (EM) plus FF (%): percentage of mares that were detected non-pregnant on Day 39 post-ovulation; overall fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
244
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
Table 2 Effects of reproductive status on measures of reproductive efficiency in Thoroughbred mares. Reproductive parameters
Reproductive status Foaling (n = 713)
Barren (n = 155)
Maiden (n = 101)
Rested (n = 62)
Aborted (n = 85)
Repeated (n = 50)
Management of estrus No. oestrous cycles No. matings per oestrus (S.D.) No. matings per Day 16 conception (S.D.)
1156 1.45 (0.44) 2.74 (0.61)
287 1.44 (0.73) 3.27 (0.68)
169 1.49 (0.88) 2.71 (1.04)
115 1.45 (0.91) 3.48 (0.68)
167 1.46 (0.78) 3.20 (0.83)
82 1.50 (0.82) 3.24 (0.88)
Pregnancy results Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Day 16 pregnancies per season (%) Un-detected EEM plus FF (%) Late embryonic losses (%) Early fetal losses (%) Mid-fetal losses (%) Late fetal losses (%) Overall EM plus FF (%) Overall fetal losses (%) Overall detected pregnancy losses (%) Mares did not produce a foal (%) Mares produced a live foal (%)
53.03 48.53ac 44.46a 85.97 14.03 8.48 2.61 2.77a 2.28 21.32 7.67a 16.15a 27.91ac 72.09ac
43.90 37.63b 33.80b 81.29 18.71 14.29 1.59 4.76 2.38 30.32a 8.73 23.02 37.42 62.58
55.03 52.66c 46.75 92.08 7.92 4.30 4.30 4.30 2.15 11.88b 10.75 15.05 21.78a 78.22a
41.74 34.78ab 30.43 77.42 22.58 16.67 4.17 6.25 0.00 35.48a 10.42 27.08 43.55c 56.45c
45.51 40.12 31.74b 89.41 10.59 11.84 3.95 11.84b 2.63 21.18 18.42b 30.26b 37.65 62.35
46.34 37.80 31.71 76.00 24.00 18.42 2.63 5.26 5.26 38.00a 13.16 31.58 48.00b 52.00b
Values in the same row with different letters (a–c) or lacking a common letter differ significantly: Bonferroni (P < 0.003); S.D. (standard deviation). Day 16 pregnancies per season (%): percentage of mares detected pregnant on day 16 post-ovulation during the season; un-detected early embryonic mortality (EEM) plus fertilization failure (FF) (%): percentage of mares that were detected non-pregnant on Day 16 post-ovulation; late embryonic losses (%): percentage of mares that lost their Day 16 pregnancies between Days 16 and 39 post-ovulation; early fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 40 and 90 post-ovulation; mid-fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 91 and 198 post-ovulation; late fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Days 199 and live foaling; overall embryonic mortality (EM) plus FF (%): percentage of mares that were detected non-pregnant on Day 39 post-ovulation; overall fetal losses (%): percentage of mares that lost their Day 16 pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
associated with spontaneous ovulation (Table 3). However, the number of matings per oestrus and matings per Day 16 pregnancy were significantly reduced when ovulation was induced hormonally (P < 0.001). 3.2. Pregnancy losses Overall 31.05% of the total mares failed to produce a foal and a major proportion of these were contributed by unobserved EEM plus FF (Table 1). Collectively, the overall EM plus FF accounted for 75% of mares that did not produce
a foal. The overall percent fetal and observed pregnancy losses were found to be 9.26% and 19.11%, respectively. Further, the late embryonic mortality (observed between Days 16 and 39) constituted more than 50% of the overall detected pregnancy losses (Table 1). When the chronic aborters and chronic barren mares were excluded from the analysis, overall percent EM plus FF occurred between Days 0 and 39 was analyzed as 18.80%, whereas overall percent detected pregnancy losses were found to be 15.27%. The incidence of percent undetected EEM plus FF was much higher (P < 0.0001) in mares age ≥18 years than
Table 3 Effects of hormonal induction of ovulation on reproductive parameters in 253 Thoroughbred mares surveyed over a period of 7 years. Reproductive parameters
No. oestrous cycles (% of total) No. matings (% of total) No. 16-day pregnancies (% of total) No. matings per oestrus ± S.D. No. matings per Day 16 pregnancy ± S.D. Day 16 pregnancies per oestrus (%) Day 39 pregnancies per oestrus (%) Foaling per oestrus (%) Late embryonic losses (%) Overall Fetal losses (%) Overall detected pregnancy losses (%) Detected pregnancies produced a live foal (%)
Type of ovulation Induced
Spontaneous
370 (18.72) 464 (16.13) 202 (20.32) 1.25a ± 0.49 2.30a ± 0.53 54.59 49.46 45.95 9.41 6.43 15.84 84.16
1606 (81.28) 2412 (83.87) 792 (79.68) 1.50b ± 0.74 3.05b ± 0.75 49.32 44.40 39.48 9.97 9.97 19.95 80.05
Values in the same row with different letter (a and b) are significantly different: Bonferroni (P < 0.001); S.D. (standard deviation). Overall fetal losses (%): percentage of mares that lost their pregnancies between Day 40 and live foaling; overall detected pregnancy losses (%): percentage of mares that lost their Day 16 pregnancies between Day 16 and live foaling.
BL
20 (40.00) 30 (60.00) 18.66 ± 2.84 15 29 41 (87.23) UL UL
4 (28.57)
Both Single
BL
Manual crushing
UL
Spontaneous/simultaneous reduction of conceptuses
BL
Prostaglandin termination
UL
3–7 and 8–12 years old mares. Furthermore, the overall percent EM plus FF were significantly lower in mares at ages 3–7 years (16.38%) and 8–12 years (21.53%) than ≥18 years old (54.55%). Mares aged ≥18 years demonstrated the greater (P < 0.001) percent late embryonic losses than 3–7- and 8–12-year age groups. Although, no differences were observed in overall fetal losses, but the percentage of mid-fetal losses (20.00%) and overall percent detected pregnancy losses (46.43%) were much higher in ≥18 years old mares compared to other age groups (P < 0.008; Table 1). Regarding mare status, undetected EEM plus FF and percent late embryonic losses were similar (P > 0.003) across all the groups. The overall percent EM plus FF was lower in maiden mares (11.88%; P < 0.001) than repeated (38.00%), rested (35.48%) and barren (30.32%) mares. Aborted mares showed higher percent mid-fetal as well as overall percent fetal and detected pregnancy losses than foaling mares (P < 0.003; Table 2). Further, greater proportion of repeated (48.00%) and rested (43.55%) mares did not produce a foal compared to maiden mares (21.78%; P < 0.003). No significant differences in terms of percent overall detected pregnancy losses and fetal losses were observed with the number of matings per oestrus, induced/spontaneous oestrus and ovulation, stud farm surveyed, and month of mating or the breeding year.
245 6 (50.00) 6 (50.00) 24.51 ± 1.98 0 0 (0)
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
BL
1 (7.14) 19.42 ± 3.17 0 0 (0) 9 (64.29) 26 (86.67) 4 (13.33) 21.15 ± 3.10 24 3 26 (86.67)
Outcome
Type of fixation: UL: unilateral; BL: bilateral; UTB: uterine body.
A total of 108 multiple pregnancies (106 twins and 2 triplets) were recorded in the study with an overall incidence of 5.40% of the total mated oestrus (10.70% of the total pregnancies; 9.14% of mare years). Amongst the twin pregnancies, 61 (57.57%) were unilateral, 44 (41.50%) were bilateral and 1 case was fixed in uterine body. The fate of multiple pregnancies is given in Table 4. The percent late embryonic losses in twin pregnancies were higher (P = 0.0016) than the overall singleton pregnancies (21.98% vs. 8.64%, respectively). There was a 15% increase in the success rate of manual crushing when two concepti were
Number of twins (percentage) Mean day of diagnosis/intervention ± S.D. No. Day 39 pregnancies No. foaling (percentage)
3.4. Multiple pregnancies
Table 4 Outcome of twin pregnancies in 253 Thoroughbred mares over a period of 7 years.
The overall live foaling rate was 68.95%. Foaling rates were higher (P < 0.0001) for mares aged 3–7 years (76.55%) than for mares at ages 13–17 years (61.99) and ≥18 years (34.09%; Table 1). Similarly, mares at ages 3–7 and 8–12 years showed more foaling per oestrus than ≥18-year olds (Table 1). When compared by reproductive status, foaling rates were significantly lower in repeated (52.00%) mares than foaling (72.09%) and maiden (78.22%) mares (Table 2). Further, significantly more foaling rates were observed in maiden than rested mares (P < 0.003). The percent foaling per oestrus was significantly higher in foaling mares compared to barren and aborted mares (P < 0.003; Table 2). The percent foaling per oestrus did not differ significantly in mares covered for ≤2 oestrous cycles (41.82%) than in mares covered during ≥3 oestrous cycles (32.19%) per breeding season. Further, the number of matings per oestrus, type of oestrus, month of mating, stud farm and year did not affect the foaling rates (P > 0.05).
UTB
3.3. Foaling rates
246
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
distributed bilaterally. Both sets of triplet pregnancies were treated successfully by crushing two concepti on the same day. 4. Discussion To the best of our knowledge, this is the first extensive report on reproductive efficiency of Thoroughbred mares of subtropical environment from Indian subcontinent that takes into consideration the effect of age and prior reproductive history on various reproductive parameters. The overall Day 16 per cycle pregnancy rate observed (50.30%) in the present study is lower than the range (54–64%) previously reported for Thoroughbred mares from the temperate regions of world (Brück et al., 1993; Hemberg et al., 2004; Allen et al., 2007). Similarly, the foaling rates are comparatively lower than several studies, but the overall per cycle pregnancy loss rates are only slightly lower than many recent studies (Brück et al., 1993; Morris and Allen, 2002). The more frequent use of diagnostic ultrasonography at the stud farms mentioned in the reports compared with our study (with only 3/4th got scanned), somewhat explains the origin of difference in the pregnancy rates. The use of ultrasonographic examination facilitates an early diagnosis of pregnancy as well as an accurate diagnosis of uteroovarian pathologies that affect the mare fertility, which consequently alters the pregnancy rates at different days (Noakes, 2001). The identification of age as a major factor influencing the pregnancy rates in Thoroughbred mares is in agreement with several other studies (Davies Morel et al., 2005; Allen et al., 2007). The decline in fertility with age has been attributed to chronic progressive degenerative changes in the endometrium (Ricketts and Alonso, 1991) along with potential susceptibility to uterine infection arising from poor perineal conformation and uterine incompetence that is observed with senescence (Kalirajan and Rajasundaram, 2008). Our study also supported a previous finding (Morris and Allen, 2002) that resting a mare may not be advantageous to get her pregnant in the next season as higher Day 39 pregnancy rates were observed in maiden mares as compared to rested mares of the present survey. However, the effect of mare’s reproductive status on pregnancy rates is still a controversial issue as some recent studies (Hemberg et al., 2004; Allen et al., 2007) in Thoroughbred mares are supportive, while findings of Brück et al. (1993) are contradictory to our observations. It is worth noting that the bigger proportion of comparatively older (13 years) mares fell in barren (40.65%) category, whereas all of the maiden mares and 3/4th of the foaling mares were less than 13 years of age. This might be responsible for the differences in the pregnancy rates with regard to reproductive status. About 50% of the mares that did not successfully foal for two seasons failed to do so in the next seasons as well, thus culling these mares might improve overall reproductive performance of the stud farm. The observed mean number of matings/oestrus and matings per pregnancy is relatively higher than the recent surveys from other countries (Allen et al., 2007). Perhaps it reflects a difference in reproductive management for predicting the optimal time of breeding and greater will-
ingness to rebred mares that fail to ovulate 36–48 h after previous matings. Our results are in agreement with the previous studies (Davies Morel and Gunnarsson, 2000; Morris and Allen, 2002) where no effect of number of matings or inseminations on pregnancy rates was observed. A decrease in Day 16 pregnancy rate with increase in number of covered oestrous cycles reported previously by Brück et al. (1993) was not seen in our study. The use of exogenous hormones to induce ovulation had no benefit over spontaneous ovulations in terms of per cycle pregnancy rates, as also reported by Morris and Allen (2002) and Davies Morel and Newcombe (2008). However, as evident from this and other studies (Grimmett and Perkins, 2001; Allen et al., 2007) hormonal induction of ovulation reduces the number of matings per oestrus and matings required per pregnancy. This might be due to increased ovulation rate with in 48 h of administration (98%) (Camillo et al., 2004) and therefore serves as an important tool to deal adequately with the markedly increased number of mares booked to popular stallions. The Day 16 pregnancy rates did not show a significant change over different months of the breeding seasons. Therefore, we were not able to demonstrate a significant decline in reproductive performance despite a rise in temperature (35–45 ◦ C) coinciding with peak breeding period (mid-April) of Thoroughbred mares in northwestern India. Similarly, Mortensen et al. (2009) obtained an acceptable embryo recovery rates (63%) from non-exercised mares during the warmest period (>30 ◦ C) of the year in central Texas. Although, estimating fertilization rate is a prerequisite to determine the exact magnitude of EEM, but it is impractical to differentiate between undetected EEM and FF under field conditions. It is generally accepted that fertilization rate in mares is generally over 90%, and is independent of age and mares status (Ball et al., 1989). In addition, the chances of fertilization failures were further lower in our study as most of the mares were covered for more than one oestrus in a season. It is likely, therefore, that the EEM is the major causative factor for subfertility in the mares, which were detected as non-pregnant on Day 16 post-ovulation. It might be possible that most of the undetected EEM occurs due to failure of maternal recognition of pregnancy during first 16 days of gestation in mares (Roberts et al., 1996) and extent of it still needs to be ascertained. The percent late embryonic mortality observed in the current survey fell within the previously reported range (5–18%) for Thoroughbreds (Simpson et al., 1982; Malschitzky et al., 2003). A major proportion (∼75%) of pregnancy failures and losses occurred before Day 40, as reported elsewhere (Morris and Allen, 2002; Yang and Cho, 2007). The issue of increase in percent late embryonic as well as overall detected pregnancy losses and decrease in pregnancy rates with advancing age (Carnevale and Ginther, 1992) are intermingled. In addition to factors discussed earlier, older mares have more incidences of multiple uterine cysts causing reduction in uterine vascular perfusion (Ferreira et al., 2008) along with frequent delayed and irregular ovulations (Carnevale et al., 1994) that release morphologically/genetically abnormal oocytes (Carnevale et al., 1999; Rambags et al., 2005) and renders
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
them subfertile. The increase in age did not affect incidence of overall percent fetal losses as shown earlier (Brück et al., 1993). However, significant differences were observed in percent mid-fetal losses that might be associated with poor placental efficiency and compromised microplacentomes devolvement in subfertile older mares (Bracher et al., 1996; Abd-Elnaeim et al., 2006) during this period. As aborted mares lost their fetus more frequently, it indicates the need of careful management in these mares. Furthermore, it is evident in the current investigation that repeated mares experienced similar pregnancy rates as well as percent embryonic, fetal and overall pregnancy losses than other reproductive statuses. It reflects the potential success of rebreeding mares in same season after experiencing a late embryonic mortality. Hence, it is advisable to breed a mare in the same season as this may have implication for stud management where the expectation is that broodmares will produce a live foal each year. With respect to twining, the overall per cycle twin pregnancy rate was well in the range of 2.1–16.2% reported across the world (Sanderson and Allen, 1987; Newcombe, 1995). As we found a lesser use (18.72%) of exogenous use of hormones than in Thoroughbred stud farms of other (59.10%) counties like United Kingdom (Allen et al., 2007), our study does not support the work of Veronesi et al. (2003) that associated the rise in twining with more increase use of hormones. Similar to previous report (Ginther, 1989a), there were more chances of unilateral fixation of twins that will get spontaneously reduced to a singleton most likely between Days 17 and 30 of pregnancy (Ginther, 1989b; Brück et al., 1993). The percent late embryonic losses of 21.98% confirmed the previous findings (Brück et al., 1993; Yang and Cho, 2007) of greater late embryonic losses in twins than for singleton pregnancy. The success rate of manual compression was 87.04% and is comparable to various reports (Merkt and Jöchle, 1993; Hemberg et al., 2004). However, we did not observe a difference between the percent late embryonic and fetal losses in both spontaneously reduced and manually crushed twin pregnancies, which is in contrast to reported increase in fetal losses after manual crushing (Brück et al., 1993). The 15% difference of bicornuate compared to unicornuate success rate of ‘pinching’ may be explained by increased ease of manipulation and/or reduced risk of damaging the neighboring conceptus. The high success of manually reducing twins to singleton may consequently increase the overall reproduction indices as such pregnancies have a chance to terminate with birth of a sound and well-developed foal (Ricketts and Young, 1990; Górecka and Jezierski, 2003). Besides the factors discussed above, other confounding variables that may affect the reproductive performance of mares are stallion’s fertility, nutrition and management of stud farms. So far, the studies on stallion fertility (Davies Morel and Gunnarsson, 2000; Morris and Allen, 2002) have been inconclusive over its effects on fertility rates. While, a long term restricted nutrition may lower mare fertility (Niekerk van and Niekerk van, 1998; Henneke et al., 1984). However, in our study any nutritional effect on reproductive performance would have been minimal as the data was collected from well-organized Thoroughbred stud
247
farm where as a standard practice the nutrition is, though not specified, considered to be good. Both of the above mentioned factors were not analyzed in this study since they can be thoroughly investigated in a controlled study only. 5. Conclusion In summary, no effect of summer stress on fertility of mares was evident, therefore a comparatively lower reproductive performance of Thoroughbreds mares bred under Indian subtropical conditions than mares of temperate regions might be due to the differences in breeding management. Further, mare age and her reproductive status strongly influenced the reproductive efficiency. In order to improve the overall reproductive performance of a stud farm, it is advisable to rebreed the mare that had lost its earlier pregnancy in the same season, and cull the chronic barren and habitual aborter mares. Acknowledgements The authors are grateful to the veterinarians, owners, staff and management of the surveyed stud farms, for access to their records and help with extraction of relevant information. Dr. G.V.P. Ravi Kumar, Assistant Professor, Department of Animal Breeding and Genetics, GADVASU, Ludhiana, Punjab, India is acknowledged for helping with statistical analysis. References Abd-Elnaeim, M.M.M., Leiser, R., Wilsher, S., Allen, W.R., 2006. Structural and haemovascular aspects of placental growth throughout gestation in young and aged mares. Placenta 27, 1103–1113. Allen, W.R., Brown, L., Wright, M., Wilsher, S., 2007. Reproductive efficiency of Flatrace and National Hunt Thoroughbred mares and stallions in England. Eq. Vet. J. 39, 438–445. Ball, B.A., Little, T.V., Hillman, R.B., Woods, G.L., 1989. Survival of Day 4 embryos from young, normal mares and aged, sub fertile mares after transfer to normal recipient mares. J. Reprod. Fertil. 85, 187–194. Bracher, V., Mathias, S., Allen, W.R., 1996. Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Eq. Vet. J. 28, 180–188. Brück, I., Anderson, G.A., Hyland, J.H., 1993. Reproductive performance of Thoroughbred mares on six commercial stud farms. Aust. Vet. J. 70, 299–303. Camillo, F., Pacini, M., Panzani, D., Vannozzi, I., Rota, Al, Aria, G., 2004. Clinical use of twice daily injections of buserelin acetate to induce ovulation in the mare. Vet. Res. Commun. 28, 169–172. Carnevale, E.M., Ginther, O.J., 1992. Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology 37, 1101–1115. Carnevale, E.M., Bergfelt, D.R., Ginther, O.J., 1994. Follicular activity and concentrations of FSH and LH associated with senescence in mares. Anim. Reprod. Sci. 35, 231–246. Carnevale, E.M., Uson, M., Bozzola, J.J., King, S.S., Schmitt, S.J., Gates, H.D., 1999. Comparison of oocytes from young and old mares with light and electron microscopy. Theriogenology 51, 299. Davies Morel, M.C.G., Gunnarsson, V., 2000. A survey of the fertility of Icelandic stallions. Anim. Reprod. Sci. 64, 49–64. Davies Morel, M.C.G., Newcombe, J.R., 2008. The efficacy of different hCG dose rates and the effect of hCG treatment on ovarian activity: ovulation, multiple ovulation, pregnancy, multiple pregnancy, synchrony of multiple ovulation; in the mare. Anim. Reprod. Sci. 109, 189–199. Davies Morel, M.C.G., Newcombe, J.R., Swindlehurst, J.C., 2005. The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare. Theriogenology 63, 2482–2493. Engelken, T.J., 1999. Reproductive health programs for beef herds: analysis of records for assessment of reproductive performance. In:
248
S. Sharma et al. / Animal Reproduction Science 117 (2010) 241–248
Youngquist, R.S. (Ed.), Current Therapy in Large Animal Theriogenology. W.B. Saunders Co., Philadelphia, pp. 451–456. Ferreira, J.C., Gastal, E.L., Ginther, O.J., 2008. Uterine blood flow and perfusion in mares with uterine cysts: effect of the size of the cystic area and age. Reproduction 135, 541–550. Ginther, O.J., 1989a. Twin embryos in mares. I. From ovulation to fixation. Eq. Vet. J. 21, 166–170. Ginther, O.J., 1989b. Twin embryos in mares. II. Post fixation embryo reduction. Eq. Vet. J. 21, 171–174. Ginther, O.J., Gastal, E.L., Gastal, M.O., Beg, M.A., 2004. Seasonal influence on equine follicle dynamics. Anim. Reprod. 1, 31–44. Górecka, A., Jezierski, T., 2003. Effect of single vs multiple ovulations on oestrus behavior and pregnancy rate in Thoroughbred mares. Animal Science Papers and Reports, vol. 21. Institute of Genetics and Animal ˛ Breeding, Jastrzebiec, Poland, pp. 27–33. Grimmett, J.B., Perkins, N.R., 2001. Pregnancy and twinning rates in Thoroughbred mares following the administration of human chorionic gonadotrophin (hCG). N. Z. Vet. J. 49, 94–100. Hemberg, E., Lundeheim, N., Einarsson, S., 2004. Reproductive performance of Thoroughbred mares in Sweden. Reprod. Domest. Anim. 39, 81–85. Henneke, D.R., Potter, G.D., Kreider, J.L., 1984. Body condition during pregnancy and lactation and reproductive efficiency in mares. Theriogenology 21, 256–258. Ju, J.C., Tseng, J.K., 2004. Nuclear and cytoskeleton alterations of in vitro matured porcine oocytes under hyperthermia. Mol. Reprod. Dev. 68, 125–133. Kalirajan, R., Rajasundaram, R.C., 2008. Incidence of endometritis in relation to age and Caslick index in mares. Indian Vet. J. 85, 893–894. Kranzler, G., Moursund, J., 1999. Statistics for the Terrified, 2nd ed. Prentice Hall, Upper Saddle River, pp. 120–125. Malschitzky, E., Schilela, A., Mattos, A.L.G., Garbade, P., Gregory, R.M., Mattos, R.C., 2003. Intrauterine fluid accumulation during foal heat increases embryonic death. Pferdeheilkunde 19, 246–249. Marai, I.F.M., El-Darawany, A.A., Fadiel, A., Abdel-Hafez, M.A.M., 2007. Physiological traits as affected by heat stress in sheep—a review. Small. Rumin Res. 71, 1–12. Merkt, H., Jöchle, W., 1993. Abortions and twin pregnancies in Thoroughbreds: rate of occurrence, treatments and prevention. J. Eq. Vet. Sci. 13, 690–694. Morris, L.H.A., Allen, W.R., 2002. Reproductive efficiency of intensively managed Thoroughbred mares in Newmarket. Eq. Vet. J. 34, 51–60.
Mortensen, C.J., Choi, Y.H., Hinrichs, K., Ing, N.H., Kraemer, D.C., Vogelsang, S.G., Vogelsang, M.M., 2009. Embryo recovery from exercised mares. Anim. Reprod. Sci. 110, 237–244. Nagamine, Y., Sasaki, O., 2008. Effect of environmental factors on fertility of Holstein–Frisian cattle in Japan. Livest. Sci. 115, 89–93. Newcombe, J.R., 1995. Incidence of multiple ovulations and multiple pregnancies in mares. Vet. Rec. 137, 121–123. Niekerk van, F.E., Niekerk van, C.H., 1998. The effect of dietary protein on reproduction in the mare. VII. Embryonic development, early embryonic death, foetal losses and their relationship with serum progestagen. J. S. Afric. Vet. Assoc. 69, 150–155. Noakes, D., 2001. Pregnancy and its diagnosis. In: Noakes, D.E., Parkinson, T.J., England, G.C.W. (Eds.), Arthtur’s Veterinary Reproduction and Obstetrics. W.B. Saunders Company, Philadelphia, pp. 69–118. Rambags, B.P., Krijtenburg, P.J., Drie, H.F., Lazzari, G., Galli, C., Pearson, P.L., Colenbrander, B., Stout, T.A., 2005. Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87. Ricketts, S.W., Young, A., 1990. Thoroughbred mare fertility. Vet. Rec. 128, 68. Ricketts, S.W., Alonso, S., 1991. The effect of age and parity on the development of equine chronic endometrial disease. Eq. Vet. J. 23, 189–192. Roberts, R.M., Xie, S., Mathialagan, N., 1996. Maternal recognition of pregnancy. Biol. Reprod. 54, 294–302. Sanderson, M., Allen, W.R., 1987. Reproductive efficiency of Thoroughbred mares in the UK. In: Proceedings of the 9th Bain-Fallon Memorial Lectures. Australian Equine Veterinary Association, Sydney, Australia, pp. 31–41. Schulman, M.L., Marlow, C.H., Nurton, J.P., 2003. A survey of reproductive success in South African Thoroghbred horse breeding from 1975 to 1999. J. S. Afric. Vet. Assoc. 74, 17–19. Simpson, D.J., Greenwood, R.E., Ricketts, S.W., Rossdale, P.D., Sanderson, M., Allen, W.R., 1982. Use of ultrasound echography for early diagnosis of single and twin pregnancy in the mare. J. Reprod. Fertil. Suppl. 32, 431–439. Veronesi, M.C., Battocchio, M., Faustini, M., Gandini, M., Cairolia, F., 2003. Relationship between pharmacological induction of estrous and/or ovulation and twin pregnancy in the Thoroughbred mares. Domest. Anim. Endocrinol. 25, 133–140. Yang, Y.J., Cho, G.J., 2007. Factors concerning early embryonic death in Thoroughbred mares in South Korea. J. Vet. Med. Sci. 69, 787–792.