Factors associated with abnormal resumption of ovarian activity after calving of Holstein-Friesian cows reared in northern Algeria

S Souames, A Abdelli¹ and Z Berrama

High National Veterinary School of Algiers, Laboratory of animal health and production, Issad Abbes, Oued Smar Algiers, Algeria
samir_souames@yahoo.fr
¹ University of Saad Dahleb, Blida, Faculty of Veterinary Science, Laboratory of biotechnology related to animal reproduction, BP 270 Ouled Yaïch, 09000, Blida, Algeria.

Abstract

The objectives of the present study were to identify the factors influencing the resumption of luteal activity, to describe the incidence of different categories of postpartum ovarian activity and to investigate the relationships among parity, calving season, body condition score (BCS) at calving, BCS loss from calving to 30 days of lactation (DIM), and abnormal resumption of ovarian cycles postpartum of 84 Holstein-Friesian cows in northern Algeria. Blood samples were collected on days 30, 42 and 54 after calving and serum progesterone concentrations were measured by enzyme immunoassay to determine the luteal activity (≥ 1ng/mL) and different types of luteal dysfunctions in cows. The luteal activity was estimated at 39% at 30 DIM, 57% at 42 DIM and 69% at 54 DIM. The onset of luteal activity was influenced by milk production at 30 DIM. Cows producing less than 3000 kg of milk per year were 1.43 times more likely to have early luteal activity. However, no significant influence was reported at 42 and 54 DIM. 38%, of cows had normal resumption and 62%, had abnormal cyclicity, where 31 had delayed first ovulation and 31%, presented prolonged luteal phase. Using multiple ordinary logistic regressions, significant associations between parity, calving season and abnormal ovarian cyclicity were identified. Primiparous cows were 6.6 times more likely to have delayed first ovulation as multiparous cows (OR=7.60, p<0.05). Calving in cold season increased significantly the risk for delayed of first ovulation (OR= 12.68, p<0.01) and prolonged luteal phase (OR=8.85, p<0.01). In conclusion, more than half of the cows presented abnormal resumption of ovarian cyclicity which was influenced by parity and calving season.

Keywords: calving season, dairy cow, ovarian cyclicity, parity, postpartum, reproduction

Introduction

One of the crucial events to regain the maximum breeding potential of postpartum dairy cows is the early resumption of ovarian cyclicity. The aim is to achieve calving to first service (waiting period) and conception intervals (open days) of 55 and 85 days respectively, so that calving to calving intervals are maintained at 365 days. In confinement herds Northern Algeria, subsequent reproductive performance in lactating cows is declined, as reflected by prolonged open days and calving to calving intervals (Madani et al 2008). Thus, the increased frequency of abnormal resumption of ovarian activity after calving such as delayed first ovulation and prolonged luteal phase is associated with degradation of reproductive performance (Petersson et al 2006).The causes of this ovarian dysfunctions are multifactorial involving parity, season of calving, severes body condition score (BCS) loss, negative energy balance, milk production yield and clinical diseases (Opsomer et al 2000; Meikle et al 2004; Lucy 2008 and Kacar et Kaya 2014). The aims of the present study were to identify the factors influencing the resumption of luteal activity, to describe the incidence of different categories of postpartum ovarian activity and to investigate the relationships among parity, calving season, BCS at calving, BCS loss from calving to 30 days after calving, and abnormal resumption of cyclicity after calving in Holstein-Friesian cows in Northern Algeria.

Materials and methods

Animals and herd

The study was conducted on 84 Holstein-Friesian cows (ranged from 2 to 11 years) reared in the Technical Institute of Livestock Breeding, in Baba Ali-Algiers (Longitude 3.067° and Latitude 36.667°). The area has Mediterranean climate with two distinct seasons, a warm summer (with peak temperatures reaching 33°C) and cold winter (with a minimum temperature below freezing) and a pluviometry comprised between 600 and 800 mm/year. Cows were kept in the tie-stall barns and fed forage (sorghum, berseem, corn silage and alfalfa hay), concentrate (corn, barley, wheat bran) and commercial concentrate for lactation with trace minerals and vitamins. Cows were machine-milked twice daily and the average 305 days milk production was 3414±1186 kg (ranged from 1950 to 6600 kg).

Blood sampling and progesterone assay

Blood samples were collected after morning milking from the coccygeal vein into vacutainer tube without anticoagulant. Samples were centrifuged at 1,500 x g for 10 minutes. Separated serum samples were collected and stored at -20°C until assay. The luteal activity was determined by serum progesterone concentrations on days 30 (d30), d42 and d54 after parturition. Progesterone (P4) concentrations were quantified by enzyme immunoassay (ST AIA-PACK PROG, Tosoh Co, Ltd, Japan). The minimal detectable concentration (sensitivity) was estimated to be 0.1ng/mL. Intra-assay and inter-assay coefficients of variation were 9.9 and 11.3 %, respectively. A functional corpus luteum (CL) was considered to be present if serum P4 concentrations were ≥ 1ng/mL (Stevenson et al 2006). Ovulation was considered to have occurred 5 days before the first rise day of luteal activity. Cows were classified into the following three groups, based on serum P4 profiles (Shrestha et al 2004).

- Normal resumption (NR): ovulation occurred ≤ 45 days after calving, followed by regular ovarian cycles.

- Delayed first ovulation (DFO): first ovulation did not occur until ˃ 45 days after calving.

- Prolonged luteal phase (PLP): ovulation occurred ≤ 45 days postpartum, but more ovarian cycles had luteal activity for ˃ 20 days.

Clinical reproductive examination of cows

In order to control uterine involution and ovarian activity of cows, rectal palpations were conducted during blood sampling.

Body condition score assessment

Body Condition Score was measured three times: at calving (BCS0), on day 30 (BCS30) and 60 (BCS60) after calving, on a scale from 1 (very thin) to 5 (fat) with 0.5 increments. All BCS were assigned by the same operator using the visual technique developed by Edmonson et al (1989).

Milk yield

The estimated 305 days milk yields of individual cows (n=66) were obtained from the Technical Institute of Livestock Breeding, Algiers.

Statistical analysis

Prior to statistical analysis, observations were checked for unlikely values; no data were excluded for this reason. Analyses were performed with SAS Software (version 9.1.3; SAS Institute Inc, Cary, NC, USA). Descriptive statistics for qualitative and quantitative variables under study were computed. The incidences of the different types of ovarian cycles postpartum during the pre-service period across cow-level factors were expressed as percentages. The GENMOD procedure of SAS was used for analyses the effect of parity (multiparous vs. primiparous), season calving (cold vs. warm), BCS, BCS loss and total milk yield on luteal activity (at 30, 42 and 54 DIM). The BCS at calving was categorized as: high (≥ 4.0), moderate (3.0-3.5) and low (≤ 2.5), BCS loss from calving to 30 DIM was classified into two categories (≥1, < 1); season calving was grouped as cold (October to March) and warm (April to September). Total milk yield was also dichotomized into three groups (< 3000, 3000-4500 and ˃4500 kg/year). Thus, effects of these covariates on abnormal resumption (DFO and PLP) of cyclicity compared with normal resumption (NR) after calving in Holstein-Friesian cows were examined by using multiple ordinary logistic regressions of SAS. Odds Ratio (OR) and 95% confidence intervals (95%-CI) were determined.

Results

Characteristics of dairy cows

61% of cows were primiparous (2.6±0.5 years), calved generally in the cold season (57%). 56% of cows had an average BCS at calving of 3.3±0.3. For most of them, the loss of BCS between the calving and 30 DIM was estimated at 0.5 point (<1 point). For more than half of cows (53%), the average 305 days milk yields remained low (2503±228 kg per year) (Table 1).

Concentration of progesterone and ovarian activity

At 30, 42 and 54 DIM, the luteal activity was estimated at 39%, 57% and 69%, respectively. Concerning the ovarian status of cows, out of 84, only 32 cows (38%) had normal resumption of ovarian cycles postpartum, where 52 cows (62%) had an abnormal ovarian cycle with 31% of DFO and 31% of PLP (Table2).

Relationships between parity, calving season, BCS at calving, BCS loss and total milk yield on luteal activity

At 30 DIM, cows producing less than 3000 kg per year were more likely to have early luteal activity (OR =1.43, p<0.05) compared with those producing more than 4500 kg/year. However, this difference was not significant for cows producing between 3000-4500 kg per year. Also, there were no significant effects (p>0.05) of parity, calving season, BCS at calving, BCS loss and total milk yield on the luteal activity at 42 and 54 DIM (Table 3).

Incidence of different types post-partum cycles during the pre-service period across parity, season calving, BCS at calving and BCS loss groups

Results presented in Table 4 showed that the late resumption was more observed in primiparous cows than multiparous ones (39 vs 18%). Calving in cold season presented DFO and PLP compared with warm season (35 vs 25%; 36 vs 22%, respectively). 42% of cows that had calved with low BCS showed DFO compared with moderate BCS at calving (30%). The proportions of cows having lost half a point of BCS between calving-30 DIM were 37, 31 and 32% in normal resumption, DFO and PLP, respectively.

Risk factors associated with abnormal resumption of ovarian activity

In the present study, two significant risk factors associated with abnormal resumption of ovarian activity were observed (Table 5). Primiparous cows were more likely to have DFO (more than 42DIM) by 6.6 times (OR=7.60, p<0.05) than multiparous cows. However, multiparous cows were equally likely (OR=1.12, p>0.05) to have PLP than primiparous cows.

Moreover, calving in cold season increased the risk for DFO by 11.6 times (OR=12.68, p<0.05) and PLP by 7.8 times (OR=8.84, p< 0.05) compared with warm season. Moreover, the regression model did not reveal significant effects (p>0.05) of BCS at calving and BCS loss on abnormal resumption of ovarian activity after calving in Holstein-Friesian cows.

Discussion

Attaining pregnancy of dairy cows within 85 days after parturition requires an early resumption of ovarian cyclicity and onset of estrus postpartum which consequently allows high reproductive potential of dairy cows (Gautam et al 2010; Kocila et al 2013). For example, the mean interval from the calving to resumption of ovarian activity was approximately 25 to 40 days postpartum with a typical range of 17 to 50 days (Butler et Smith 1989; Staples et al 1990; Akhtar et al 2015). According to Tamadon et al (2011), 72% of cows have resumed luteal activity earlier than 45 days after calving. However, in our study, only 39% of the cows (33/84) resumed their ovarian activity at 30 days after parturition, relatively lower than that reported by Disenhaus et al (2008) (52%) and Ghanem (2016) (47.5%), but not far from reported by Galvao et al (2010) and Kalem et al (2017). The onset of luteal activity at 30DIM can be explained, in the present experiment, by low level of milk production (<3000 kg/year) (OR=1.43, p<0.05) and consequently of a less serious negative energy balance. According to the literature, the risk for delayed cyclicity was higher when milk production was high (Grimard et Disenhaus 2005; Peter et al 2009). It has been suggested that higher milk production reduces the likelihood that the first dominant follicle will ovulate (Beam et Butler 1999). On the other hand, an earlier study has found no relationship between milk production and reproduction up to 5900 kg/year (Buckley et al 2003).

Abnormal patterns of resumption of cyclicity have often been identified in Holstein-Friesian cows in numerous countries (Grimard et Disenhaus 2005; Crowe 2008). In the current study, serum levels of progesterone showed a higher incidence of abnormal ovarian cycles compared with normal ovarian cycles (62% vs 38%). Several studies have revealed similar rates, (55% vs 45% n=37) (Taylor et al 2003); (63% vs 37% n=54) (Shrestha et al 2004); (55.5% vs 44.5% n=110) (Shrestha et al 2005); (57.1% vs 42.9% n=21) (Hommeida et al 2005) and (52.5% vs 47.5% n=61) (Ghanem 2016). However, more recent studies have not confirmed these results. Indeed, a higher frequency of normal resumption of ovarian activity postpartum was reported by Ledoux et al (2011) (56.5% vs 43.5% n=239) and Tamadon et al (2011) (71.8% vs 28.2% n=71).

Delayed first ovulation and PLP were the most frequently observed problems in this study which concords with previous experiments (Petersson et al 2006; Ledoux et al 2011). Incidence of DFO (31%) was higher than  observed by Shrestha et al (2005) (24.1%), Shrestha et al (2004) (12.7%) and Ledoux et al (2011) (16.3%) but similar to that reported by Hommeida et al (2005) (33.3%). In the current study, parity and calving season were significant ( p<0.05) risk factors for DFO. Primiparous cows had 6.6 times more risk of suffering from DFO compared with multiparous cows. This relationship was in accordance with reports that primiparous cows had more days to first insemination than multiparous cows (115 vs 105 days, p<0.05) (Folnožić et al 2016). The later ovulation observed in primiparous cows can be explained, in this study, by several hypotheses as metabolic problems, calving problem and occurrence of puerperal disturbances (metritis), as previously reported by Vercouteren et al (2015). Calving in the cold season had 11.7 times more risk of suffering from DFO compared with calving in warm season. This result was also reported in a field study conducted by Opsomer et al (2000) who reported that the most unfavorable breeding season being winter, knowing that 38% of cows calving in the winter did not resume ovarian activity during the first 50 days after calving. Our results may be explained by the fact that cows were housed in stables and therefore there were feeding and locomotion problems during winter (Opsomer et al (2000). Furthermore, calving in a stable was a risk factor for abnormal ovarian function when compared with calving in pasture. However, no significant differences (p>0.05) were observed in this study, between BCS at calving, BCS loss from calving to 30 DIM and DFO.

In our experiment, incidence of PLP (31%) was higher than those observed by Ledoux et al (2011) (18.4%) and Ghanem (2016) (21.3%) but similar to that reported by Hommeida et al (2005) (28.3%) and Shrestha et al (2005) (33.6%). Calving season was the most risk factor for developing PLP. Cows calving in the cold season had 7.8 times more risk of suffering from PLP compared with cows calving in warm season. This risk factor could be associated with retained placenta, abnormal vaginal discharge, metritis, as previously reported (Opsomer et al 2000; Taylor et al 2003; Shrestha et al 2004; Kacar et kaya 2014). In addition, these puerperal pathologies may compromise the uterine ability to produce PGF2a (Baranski et al 2013). This was likely to be one of the factors predisposed to PLP in our experiment. Finally, the logistic regression model showed no significant effects (p>0.05) between PLP and parity, BCS at calving and BCS loss from calving to 30 DIM.

Conclusion

• In conclusion, high incidence of abnormal ovarian cycles was observed. Delayed first ovulation and prolonged luteal phase were the main abnormal patterns of ovarian cyclicity, wich were influenced by the parity and the calving season.
  
  
• Primiparous cows were a significant risk factor for DFO. Calving in cold season was more risk factor of suffering from DFO and PLP.
  
  
• Housing in tie-stall barns, energy deficiency, physical inactivity and clinical disorders, observed during winter calving, were considered the main causes of reproductive failure.

Conflict of interests statement

The authors declare that there is no conflict of interests regarding the publication of this article.

References

Akhtar M S, Hussain S I, Ayaz M M, Lodhi LA, Ameen M, Ullah S, Lashari MH, Farooq A A and Akhtar M 2015 Effect of Bull Exposure on the Post-partum Reproductive Efficiency in Cholistani Cows. Kafkas Univ Vet Fak Derg, 21 (1): 33-36. http://vetdergi.kafkas.edu.tr/extdocs/2015_1/37-40.pdf

Baranski W, Lukasik K, Skarzynski D, Sztachanska M, Zdunczyk S and Janowski T 2013 Secretion of prostaglandins and leukotrienes by endometrial cells in cows with subclinical and clinical endometritis. Theriogenology, 80 (7): 766-772.

Beam SWand Butler WR 1999 Effects of energy balance on follicular development and first ovulation in postpartum dairy cows. J Reprod Fertil, Suppl 54: 411-424. https://www.researchgate.net/publication/12622452

Buckley F, O’Sullivan K, Mee JF, Evans RD, and Dillon P 2003 Relationships Among Milk Yield, Body Condition, Cow Weight, and Reproduction in Spring-Calved Holstein-Friesians. J Dairy Sci 86: 2308–2319

Butler WR and Smith RD 1989 Interrelationship between energy balance and postpartum reproductive function in dairy cattle. J Dairy Sci, 72: 767–783.

Crowe M A 2008 Resumption of ovarian cyclicity in postpartum beef and dairy cows. Reprod Domest Anim, 43 (5): 20-28. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0531.2008.01210.x/epdf

Disenhaus C, Cutullic E, Blanc F, Gatien J, Agabriel J, Hetreau T, Michel G, Paccard P, Badinand F, Egal D and Ponsart C 2008 Caractéristiques comparées de la cyclicité après vêlage de différentes races bovines. Rencontre Recherche Ruminants, 15: 383-386. http://journees3r.fr/IMG/pdf/2008_12_reproduction_02_Disenhaus.pdf

Edmondson A J, Lean II, Weaver I D, Farver T, Webster G 1989 A body condition scoring chart for Holstein dairy cows. J Dairy Sci, 72: 68-78.

Folnožić I, Turk R, Đuričić D, Vince S, Meštrić ZF, Sobiech P, Lojkić M, Valpotić H and Samardžija M 2016 The effect of parity on metabolic profile and resumption of ovarian cyclicity in dairy cows. Vet Arh, 86 (5): 641-653. https://hrcak.srce.hr/file/247097

Galvao K N, Frajblat M, Butler W R, Brittin SB, Guard C L and Gilbert R O 2010 Effect of Early Postpartum Ovulation on Fertility in Dairy Cows. Short Communication, Reprod Domest Anim, 45: 207-211. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0531.2009.01517.x/epdf

Gautam G, Nakao T, Yamada K and Yoshida C 2010 Defining delayed resumption of ovarian activity postpartum and its impact on subsequent reproductive performance in Holstein cows. Theriogenology, 73: 180-189.

Ghanem M E 2016 Delayed ovarian cyclicity does not reflect blood metabolites irregularity in postpartum Holstein cows. Iran J Appl Anim Sci, 6(1): 35-42. http://www.sid.ir/FileServer/JE/1034220160109

Grimard B and Disenhaus C 2005 Les anomalies de la reprise de la cyclicité après vêlage. Le point vétérinaire, Numéro spécial Reproduction des Ruminants : maîtrise des cycles et pathologie, 36 : 16-21. https://www.researchgate.net/profile/Benedicte_Grimard/publication/279766963_Anomalies_de_reprise_de_la_cyclicite_chez_la_vache_laitiere/links/559a7d3608ae793d138196e1/Anomalies-de-reprise-de-la-cyclicite-chez-la-vache-laitiere.pdf

Hommeida A, Nakao T and Kubota H 2005 Onset and duration of luteal activity postpartum and their effect on first insemination conception rate in Lactating dairy cows. J Vet Med Sci, 67 (10): 1031-1035. http://khartoumspace.uofk.edu/bitstream/handle/123456789/20491/Onset%20and%20Duration%20of%20Luteal%20Activity.pdf?sequence=1

Kacar C and Kaya S 2014 Uterine infections in cows and effect on reproductive performance. Kafkas Univ Vet Fak Derg 20 (6): 975-982. http://vetdergikafkas.org/uploads/pdf/pdf_KVFD_L_1962.pdf

Kalem A, Hanzen C, Abdelli A and Kaidi R 2017 Body condition score, some nutritional parameters in plasma, and subsequent reproductive performance of Montbéliarde cows in Algeria. Livestock Research for Rural Development. Volume 29, Article #2. Retrieved November 21, 2017, from http://www.lrrd.org/lrrd29/1/kale29002.htm

Kočila P, Janžek A, Gračner D, Dobranić T, Đuričić D, Prvanović N, Filipović N, Gregurić G G, Bedrica L I, Marković F, Horvat M and Samardžija M 2013 Vergleich von Progesteron konzentrationen, Energie bilan zkennwertenund körperlicher Verfassungbei Milch kühenmitverschiedener Milchleistung im Puerperium Tierärztl. Umschau 68: 266-274.

Ledoux D, Touze J L, Richard C, Ponter AA, Bosc M J and Grimard B 2011 Abnormal patterns of resumption of cyclicity after calving in Holstein cows: risk factors, relationships with the ultrasound appearance of the ovaries and with gestation failure after AI. Rev Med Vet, 162 (2): 98-106. http://prodinra.inra.fr/record/46147

Lucy MC 2008 Functional differences in the growth hormone and insulin-like growth factor axis in cattle and pigs: implications for postpartum nutrition and reproduction. Reprod Domest Anim, 43:31-39. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0531.2008.01140.x/epdf

Madani T, Yakhlef H and Marie M 2008 Effect of age at first calving on lactation and reproduction of dairy cows reared in semi-arid region of Algeria. Livestock Researchfor Rural Development, 20 (6), Volume 20, Article #92. Retrieved November 21, 2017, from http://www.lrrd.org/lrrd20/6/mada20092.htm

Meikle A, Kulcsar M, Chilliard Y, Febel H, Delavaud C, Cavestany D and Chilibroste P 2004 Effects of parity and body condition at parturition on endocrine and reproductive parameters of the cow. Reproduction, 127: 727–737. http://www.reproduction-online.org/content/127/6/727.full.pdf+html

Opsomer G, Gröhn Y T, Hertl J, Coryn M, Deluyker H and De Kruif A 2000 Risk factors for postpartum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology , 53: 841-857.

Peter A T, Vos PLAM and Ambrose D J 2009 Postpartum anestrus in dairy cattle. Theriogenology,71: 1333-1342.

Petersson K J, Gustafsson H, Strandberg E and Berglund B 2006 Atypical progesterone profiles and fertility in Swedish dairy cows. J Dairy Sci, 89: 2529-2538.

Shrestha H K, Nakao T, Suzuki T, Akita M and Higaki T 2005 Relationships between body condition score, body weight, and some nutritional parameters in plasma and resumption of ovarian cyclicity postpartum during pre-service period in high-producing dairy cows in a subtropical region in Japan. Theriogenology, 64: 855-866.

Shrestha H K, Nakao T, Suzuki T, Higaki T, and Akita M 2004 Effects of abnormal ovarian cycles during pre-service period postpartum on subsequent reproductive performance of high-producing Holstein cows. Theriogenology, 61: 1559-1571.

Staples C R, Thatcher W W and Clark J H 1990 Relationship between ovarian activity and energy status during the early postpartum period of high producing dairy cows. J Dairy Sci,73: 938-947.

Stevenson J S, Pursley J R, Garverick H A, Fricke P M, Kesler D J, Ottobre J S and Wiltbank M C 2006 Treatment of cycling and noncycling lactating dairy cows with Progesterone during Ovsynch. J Dairy Sci, 89 (7): 2567-2578.

Tamadon A, Kafi M, Saeb M, Mirzaei A and Saeb S 2011 Relationships between insulin-like growth factor-I, milk yield, body condition score, and postpartum luteal activity in high-producing dairy cows. Trop Anim Health Prod, 43: 29-34.

Taylor V J, Beever D E, Bryant M J and Wathes D C 2003 Metabolic profiles and progesterone cycles in first lactation dairy cows. Theriogenology, 59: 1661-1677.

Vercouteren M M A A, Bittar J H J, Pinedo P J, Risco C A, Santos J E P, Vieira Neto A and Galvao K N 2015 Factors associated with early cyclicity in postpartum dairy cows. J Dairy Sci, 98 (1): 229-239.

Received 18 January 2018; Accepted 1 February 2018; Published 1 March 2018

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