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Revista MVZ Córdoba

Print version ISSN 0122-0268

Rev.MVZ Cordoba vol.19 no.1 Córdoba Jan./Apr. 2014

 

ORIGINAL

Risk factors for ovarian postpartum resumption in Holstein cows, under high tropical conditions

 

Factores que afectan la reactivación ovárica postparto en vacas Holstein, en el trópico alto

 

Humberto Guáqueta M,1* MV, Jorge Zambrano V,1 Ph.D, Claudia Jiménez E,1 DVSc.

1Universidad Nacional de Colombia, School of Veterinary Medicine and Animal Husbandry, Department of Sciences for Animal Health, Animal Reproduction And Herd Health Research Group. Edificio 561B, Carrera 30 No. 45-03 Bogota, Colombia.

*Correspondence: hguaquetam@unal.edu.co

Received: April 2013; Accepted: November 2013.


ABSTRACT

Objective. To evaluate the factors associated with postpartum ovarian resumption and follicular dynamics in Holstein cows under high altitude conditions (2,600 masl). Materials and methods. Forty-five Holstein cows were studied between 14 days before and 120 days after calving. Uterine involution, follicular dynamics, serum progesterone and peripartum pathologies were evaluated; additionally, body condition (BC), calving type, milk yield, were also evaluated. According to hormonal and reproductive findings, cows were classified into two groups: early ovarian resumption (EOR) or delayed ovarian resumption (DOR). Results. The occurrence of the first follicular for EOR animals (n=31) was produced on average 9.58±3.45 days postpartum and was similar to the DOR group (n=10) [10.8±4.83 days; p>0.05)]. The first postpartum ovulation occurred at 21.55±5.90 days (EOR) and was significantly delayed (48.7±27.85 days) for DOR animals (p<0.05). Thirty-six point five percent of the cows (n=f) had normal estrus cycles (18 to 24 days), while 63.5% (n=26) showed dysciclia. The factors associated with ovarian resumption and cyclicity were the loss of BC [OR=3.3, CI 95% (1.2-13.3) (p<0.05)] and lameness [OR= 9.0, CI 95% (1.2-13.3) (p<0.05)]. Conclusions. Although the emergence of postpartum follicular waves was observed early, under the experimental conditions of this study there are factors that may affect the first ovulation favoring the occurrence of anovulatory conditions. The determinant factors were low body condition and lameness.

Key words: Anovulation, ovarian follicle, postpartum (Source: DeCS).


RESUMEN

Objetivo. Evaluar los factores asociados con la reactivación ovárica y la dinámica folicular postparto en vacas de la raza Holstein bajo condiciones de altura (2600 msnm). Materiales y métodos. Cuarenta y cinco vacas Holstein fueron estudiadas entre 14 días preparto y 120 días posteriores al mismo. Fueron evaluadas la involución uterina, dinámica folicular, progesterona sérica y presentación de patologías en el periparto; adicionalmente la condición corporal (CC), tipo de parto y producción de leche. De acuerdo con los hallazgos reproductivos y hormonales, las vacas se agruparon en dos grupos: reactivación ovárica temprana (ROT) o retardada (ROR). Resultados. La emergencia de la primera onda folicular para animales ROT (n=31), ocurrió en promedio 9.58±3.45 días postparto y fue similar a los ROR (n=10) [10.8±4.83 días (p>0.05)]. La primera ovulación postparto se observó a los 21.55±5.90 días (ROT) y fue significativamente más demorada (48.7±27.85 días) para los animales ROR (p<0.05). El 36.5% de los animales (n=f) presentaron ciclos estrales normales (18 a 24 días), mientras que el 63.5% (n=26) mostraron disciclia. Los factores asociados con la reactivación ovárica y la ciclicidad fueron la pérdida de CC [OR= 3.3, IC 95% (1.2-13.3) (p<0.05)] y la presentación de cojeras [OR= 9.0, IC 95% (1.2-13.3) (p<0.05)]. Conclusiones. Aunque la emergencia de ondas foliculares postparto se presentó de manera rápida, bajo las condiciones experimentales del presente estudio, existen factores que afectan la primera ovulación favoreciendo la presentación de condiciones anovulatorias. La presentación de cojeras, y la pérdida de CC postparto fueron factores determinantes.

Palabras clave: Anovulación, folículo ovárico, postparto (Fuente: DeCS).


INTRODUCTION

Reproductive efficiency is a challenge for breeders and milk producers around the world. One of the main problems for farms is the delay in the resumption of postpartum ovarian activity. To obtain the ideal interval between calving (IBC) of twelve months, animals must conceive within 85 days after partum, which requires the normalization of their cyclicity (1). This is a critical event for achieving efficient reproductive performance and minimizing economic losses represented in the increase in the number of open days and services per conception.

Growth patterns and follicle dynamics have been widely described in postpartum bovines. While some animals did not show normal ovarian activity (anestrus), others show development and growth waves of follicles that are not ovulated, generating different types of anoestrus (2,3).

Some authors have described the emergence of the first wave (4,5); others have determined the diameter and size of the ovarian structures with respect to the development phase of the same (6). The effects of common pathologies in dairy bovines have also been investigated (mastitis, retention of fetal membranes, metritis, puerperal hypocalcemia, ketosis and lameness,) on ovarian dynamics and fertility during postpartum, reporting important relationships between the occurrence of such pathologies and poor reproductive performance (7-9).

In Colombia there have been some investigations relating to follicular dynamics and postpartum ovarian resumption, although most of them have been mainly with Bos indicus animals (10,11). The studies conducted in the country for characterizing follicular and ovarian dynamics during postpartum in high yield Holstein bovines and genetic selection are scarce (12,13).

The objectives of this study were to prospectively evaluate some of the factors associated with postpartum ovarian resumption in a specialized Holstein cow farm, under high tropical conditions and characterize postpartum ovarian resumption patterns and follicular dynamics.

MATERIALS AND METHODS

Study site and animals. The study was conducted in a dairy farm in the Sabana de Bogota, at a height of 2565 meters, with annual rainfall of 698 mm and average temperature of 14°C, which corresponds to a region of the tropics located above 2,000 masl, with low temperatures and significant changes between day and night (14). In a farm of 230 Holstein cows under a kikuyo (Pennisetum clandestinum) and ryegrass (Lollium multiflorum) rotational grazing system, supplemented with concentrate and commercial mineral salts and milked twice a day. Of the total number of animals (n=230) a sample of 45 was chosen, which were evaluated for the first time two weeks before partum, recording their general health and body condition; a record of all health events and type of calving was also made. From that moment, they were subject to clinical-reproduction examination every other day, until they received their first postpartum insemination or until 120 days from calving have been completed.

Body condition. The body condition (BC) was assessed during the entire period of the study using a scale from 1 to 5 (1=thin, 5=obese) (15). The most important days used in the BC analysis were two weeks before the expected date of partum and day 30 and 60 postpartum (2).

Milk production. Milk production was recorded using the gauges of the milking equipment (Westfalia-Surge®, mini True-test® Wellington, New Zealand). The information relevant to the productive and reproductive monitoring of the farm was stored in the Interherd® software, Version 2-10-10, of InterAgri-Animal Information Management Systems Limited, UK. (Pan Livestock Services). The data corresponding to the daily average of milk production at day 28 and 60 postpartum was collected; as well as the final production adjusted to 305 days for each animal.

Follicular dynamics and ovulation monitoring. In order to group animals in relation to the time of ovarian resumption, the general average and standard deviation (32±DE) of the days of the first postpartum ovulation was used. This data was used as a cutoff point for grouping animals into two categories: those with early ovarian resumption and ovulation before day 32 (EOR); and those with delayed ovarian resumption (DOR) since its occurrence happened after day 32 postpartum. The duration of the estrous cycle after the first ovulation was considered normal when cycles lasted between 18 and 24, or altered (dysciclia) when the interval between two consecutive estrous were less than 17 or greater than 25 days (3, 6). The resumption of ovarian activity was determined by the emergence of the first postpartum follicular wave (follicles with diameters ≥ 5 mm); dominant follicles were followed with ultrasound until atresia or ovulation. Ovulation was defined as the disappearance of the preovulatory follicle from the last follicular development wave and the subsequent emergence of a corpus luteum (CL) (16), as well as the increase in serum progesterone (P4) levels ≥ 1 ng/ml (17).

The monitoring of the reproductive clinical was carried out by rectal palpation and ultrasonography every other day; these were performed with a portable equipment (Agroscan-L® ECM, France) equipped with a 5.0 MHz linear transducer. All follicles ≥5 mm as well as luteal structures were recorded in ovarian maps, adapted in accordance with the methodology described in previous studies (4.5) and some suggested models (18). The size of follicles and corpus luteum with diameters larger than 5 mm was recorded in accordance with the methodologies described in similar studies (19-21). Ovarian structures observed from a single frozen image were measured when the maximum apparent area in each of them was visualized. The volume of the corpus luteum (VCL) was calculated using the formula VCL=4/3 x π x r3, where the radius (r) was calculated with the r=(L/2+A/2)/2 (21). Luteal activity was evidenced by the observation of two consecutive samples of serum progesterone with concentrations higher than 1 ng/ml (20-22). Data was normalized with respect to the time of the first postpartum ovulation. Anestrus was defined as the absence of luteal activity after ultrasound and confirmed by basal progesterone levels in blood (<1 ng/ml) and absence of corpus luteum (6,23).

Blood and urine samples. During the evaluations, blood samples were collected by puncturing the coccygeal vein, using vacuum tubes without anticoagulant (Vacutainer®, Becton-Dickinson, Rutherford, NJ, USA). Once collected, they were refrigerated and transported to the laboratory where they were centrifuged at 3000 rpm for 20 minutes to separate the serum, which was fractioned and stored in Eppendorf tubes at -70°C until the measurement of calcium and progesterone concentrations.

During the first and second week postpartum, two urine samples were collected with intervals of seven days between them, in order to determine the levels of ketones using reagent strips (Bayer, Reagent strips for Urianalysis: Multistix® 10SG. Siemens Healthcare Diagnostics Inc. Los Angeles, CA 90045 USA).

Serum progesterone measurement. The measurement of serum progesterone levels was carried out through the solid-phase radioimmunoassay technique (RIA), using the kits Coat-A-Count Progesterone® (Siemens Healthcare Diagnostics Inc. Los Angeles, CA 90045 USA), with an analytical sensitivity of 0.02 ng/ml. and cross reactivity of 100% for P4 but very low with other naturally produced steroids or drugs present in the sample. Progesterone concentrations were measured in aliquots separated according to the procedures suggested by the producers of the kit, in the hormone laboratory of the Faculty of Veterinary Medicine and Animal Husbandry of Universidad Nacional de Colombia. The results were printed, expressed in radioactivity levels, so they had to be subsequently transcribed to the RIAPC® software to allow their quantification in nanograms per milliliter (ng/ml). Intra-assay and inter-assay variation coefficients were 7.8% and 4.7%, respectively.

Detection of estrus and artificial insemination. The detection of estrus was performed through the visual observation method, three times a day, in periods of at least 15 minutes each, where any breeding activity of or attempts thereof were registered, as well as some of the signs of estrus (vaginal discharges or presence of mucus, sniffing and following of other cows). Estrus was defined as the permanence of an animal to be mounted by another for a few seconds a conduct known as static breeding (24). The voluntary waiting period (VWP) established in the farm was 50 days. All animals that met the VWP, having approved the previous reproductive assessments, were inseminated once detected in estrus, in accordance with the am/pm system (24,25).

Description of variables. Variables were categorized as follows: 1) body condition (BC) before and after partum (1-5 scale); 2) calcium serum concentration before and after partum (mg/dL), 3) calving type (normal or dystocias); 4) number of births (first and second birth versus animals with three or more births); 5) diameter of ovarian structures (follicles ≥ 5mm and corpora lutea (mm), 6) diameter of horns at the fork (mm); (7) daily milk production (Kg/milk/cow/day); 8) occurrence of puerperal disease: hypocalcemia, ketosis, retained placenta, puerperal metritis, mastitis, ovarian cysts, lameness and fever; 9) application of postpartum treatments; 10) serum progesterone concentrations (ng/ml in blood); and 11) days to the first postpartum ovulation.

Statistical analysis. The information obtained from the ultrasound tests of ovaries and serum progesterone concentrations were initially analyzed by descriptive statistics, comparison of averages and establishing differences between the animal groups. The data was normalized with respect to the time of ovulation and subsequently analyzed using the repeated measures General Linear Model. The analysis of the factors associated with postpartum ovarian resumption such as CC, serum calcium, calving type, number of births, peripartum metabolic diseases (hypocalcemia or ketosis), pathologies and milk production, was first carried out through a univariate analysis with 2 x 2 contingency tables; then the variables that were significant according to the Chi square test (p<0.05) were selected, these variables were included in a final Binary Logistic Regression model to determine the variables associated with the first postpartum ovulation. The strength of the association was estimated by calculating the Odds Ratio (OR) with its respective 95% confidence interval. Every p<0.05 value was considered significant. Statistical analyses were performed using SPSS® software version 17.0.

RESULTS

Follicular dynamics and first postpartum ovulation. The emergence of the first postpartum follicular wave was observed on average on day 10.1±3.45. Thirty-nine percent of animals (n=16) showed such emergence between days 4 and 8 postpartum, while in 46.3% (n=19) it was observed between days 9 and 13, and in 14.6% (n=6) it took place between day 14-20. All the animals resumed their follicular dynamics before day 20 postpartum.

The average number of days to the first ovulation was 24.26±7.84 (range from 13 to 41). For statistical analysis purposes and based on this average plus one standard deviation, day 32 was defined as the average number of days to the first postpartum ovulation, which was used as a cutoff point for defining two categories: EOR animals (n=31) and DOR animals (n=10), (Table 1).

Overall, the interval between calving and the first ovulation, and calving and the following ovulation (second, third and fourth) between EOR and DOR individuals, were statistically different (p<0.05). However, there were no significant differences in the interval between two consecutive ovulations (interovulatory) between animals with EOR and DOR (p>0.05). Individuals in the EOR group had a smaller ovulatory follicle diameter both in the first as in the subsequent four cycles (18.07±5.0 mm, 21±4.4 mm, 21.8±3.2 mm and 21.9±3.2 mm), when compared with those of the DOR group during the same periods (23.1±5.2 mm, 23.8±5.9 mm, 24.8±8.8 mm and 35.4±10.4 mm). This difference in ovulatory follicle diameter was not significant at the time of the first postpartum ovulation, but it did in the three subsequent ovulations (p≤0.05).

Of a total of 146 ovulations recorded with ultrasound only 53 estrus were visualized, which corresponds to a detection percentage of 36%.

Post-ovulation ovarian activity. A total of twenty-seven animals (65.9%) showed normal cyclicity after the first postpartum ovulation with estrus cycles of 18-24 days, while 34.16% (n=14) were acyclic during the first 67 days, including anovulation by ovarian cystic conditions (n=2), Anovulation by persistent CL (n=8) and follicular development with inability to achieve ovulatory diameter (n=4).

CL volume y and serum P4 levels. There were no statistical differences in serum P4 concentrations amid animals in the EOR group as compared with those of the DOR group, during the 15 days following their first postpartum ovulation (p>0.05); however, the latter group was characterized by prolonged luteal phases (sustained levels of P4≥1 ng/ml) for periods between 24 and 32 days (Figure 1).

The maximum CL volume was 5.000 ± 400 mm3 between days 12 and 16 of the cycle following the first postpartum ovulation in EOR animals. DOR animals showed CL with prolonged duration, the maximum volume of which was 8.000 ± 400 mm3 and remained for more than 30 days after the first ovulation (p<0.05) (Figure 2).

Body condition. A decrease in the body condition (BC) of all animals in the study was observed during the first 60 dpp. The prepartum BC averaged 3.3±0.22 (range from 2.9 to 3.7), while the averages on days 28 and 60 postpartum were [2.5±0.18 (range from 1.9 to 2.9) and 2.4±0.24 (range from 1.8 to 2.8), (p<0.05)].

There were no statistical differences in the prepartum BC in the EOR (3.3±0.19) and DOR group (3.2±0.27) (p>0.05); however, differences between them during postpartum were observed. DOR animals lost more BC (2.3±0.24) than EOR animals (2.5±0.15) when the evaluation was carried out on day 28 (p≤0.05); although by day 60 postpartum this difference was no longer detected, EOR (2.3±0.18) vs. DOR (2.2±0.19) (p>0.05).

Milk production. Milk production on day 28 in EOR animals averaged 32.65±6.1 liters, similar to DOR animals that averaged 33.30±5.6 liters (p>0.05). Production averages on day 60 were 36.61±6.9 and 35.50±4.6 liters for animals of the EOR and DOR group respectively (p>0.05). There were no significant differences in lactations adjusted to 305 days for animals of the EOR group (8.404.9±1.619 liters) as compared with the DOR group (8.282.4±1.535 liters) (p>0.05).

Factors associated with the first postpartum ovulation. The prevalence observed of pathologies associated with peripartum was as follows: 34.1% of animals had fever during their first postpartum week (n=14); 19.5% showed clinical hypocalcaemia (down cows) (n=8); 58.5% subclinical hypocalcemia (n=24); 26.8% dystocia (n=11); 24.3% retained placenta (n=10); 14.6% puerperal metritis (n=6); 36.5% endometritis (n=15); 29.2% ovarian cystosis (n=12); 34.1% mastitis (n=14) and 21.9% lameness (n=9).

The univariate analysis showed that fever during the first postpartum week, low serum calcium levels during the same period, metabolic diseases (ketosis or hypocalcemia), application of postpartum treatments, other puerperium pathologies such as retention of fetal membranes, puerperal metritis, mastitis, or ovarian cysts, were not statistically associated with the first postpartum ovulation and subsequent cyclicity resumption (p>0.05). Likewise, ketosis was excluded both from the univariate and the multivariate analysis, since none of the animals showed positive results. Secondly, it was noted that the presentation of dystocia (OR=2.2; CI 0.5-10.5; p<0.5), the decrease of BC (<2.5) (OR=3.3; CI 1.1-13.8; p<0.05) and the presence of lameness (OR=10.3; CI 1.2-92.2; p<0.05) were factors associated with delays in the first postpartum ovulation (Table 2).

The final multivariate binary logistic regression analysis model determined that the risk factors associated with the delay of the first postpartum ovulation were, loss of body condition until reaching a score of less than 2.5 (OR=3.3, CI 95% (1.2-13.3) (p<0.05) and lameness (OR=9.0, CI 95% (1.2-13.3) (p<0.05). (Table 3).

DISCUSSION

This research evaluated the follicular dynamics in dairy cattle under high tropical conditions, before and after the first postpartum ovulation, as well as the degree of association with some of the most frequently pathologies reported during peripartum. The results of the study allowed to elucidate ovarian resumption patterns and determine some risk factors associated with postpartum ovarian resumption under such conditions.

The emergence of the first follicular wave was observed on average on day 10.1±3.45 (range from 4 to 22) postpartum, this being consistent with previous results that reported the emergence of the first dominant follicle, which is not always ovulatory, at day 7.0±0.9 (26) and 11.6±2.0 (range from 5 to 39) after partum (17,27). In this study, sixteen of the animals (39.2%) showed the emergence of the first early follicular wave development (days 4 to 8), nineteen of them (46.3%) between days 9 and 13, and finally six animals (14.6%) between day 14 and 22 postpartum; showing a distribution consistent with the results of other studies (5-6).

The days to the first ovulation in this study averaged 24.26 ± 7.84; these results are slightly lower than those described by other researchers in different latitudes (27), and under different production systems (grazing vs. housing).

The percentage of detection of estrus observed in this study was 36%, which coincides with other studies (28). The proportion of animals classified in anestrus, using for this purpose the estrus detected, was 64% (26/41), this differs from the result obtained by classifying animals based on ultrasound findings (CL present) and with the measurement of P4, which yielded lower results corresponding to 11% (5/41) of animals. This problem contributes to increase the percentage of animals that commonly are reported in anestrus, when sometimes there can be problems associated with the inadequate detection of estrus, and not strictly by inactive ovaries or true anestrus (3), or alterations in the follicular development, such as anovulation and absence of CL, a situation that has also been raised by other authors (29). It is possible to speculate that these differences can be attributed to ovulations without manifestation of estrus signs (24), or the presentation of low-intensity and short-duration estrus, making their expression and behavior not evident (23), probably due to changes in the metabolism of steroidal hormones and follicular fluid, proposed by some authors in high yield dairy cows (15,22).

The CL volume in animals with DOR was higher than those with EOR, which does not seem to affect P4 concentrations during the first 16 days after the first ovulation, probably due to the fact that production levels were high and therefore progesterone would metabolize in a similar manner (21). There were no statistical differences in serum concentrations of P4 among animals with EOR and DOR during the same period of time (p>0.05); however, the latter group was characterized by prolonged luteal phases. These data are consistent with a previous report (17), in which two-thirds of the animals presented delayed postpartum ovarian cyclicity resumption.

In this study was observed a decrease in the BC score of cows during the first 60 days postpartum, which did not appear to affect the occurrence of first follicular wave, since it was observed that all animals started producing follicles before day 20. Conversely, the return to cyclicity after the first postpartum ovulation was affected, allowing to observe that animals whose BC dropped to a value less than or equal to 2.5 on day 32 postpartum, were 3.3 times more likely to have delayed ovulation (OR = 3.3, CI 95% (1.2-13.3) (p<0.05). This period is critical due to the increased demand for nutrients required for milk production (2), and the mobilization of fat from body reserves by the gap occurring between metabolic demands and the intake of dry material in early postpartum (15,29), especially if the nutritional handling during the transition period is not appropriate (1), a common situation in certain grazing systems.

In this study the main problem found in animals was associated with various alterations in cyclicity subsequent to the first ovulation, where anovulation could be first observed by cystic ovary conditions; in some cases probably associated with energy or nutritional disturbances or imbalances (2, 29). Secondly, the inability of the follicle to achieve ovulatory diameter was observed, a situation that has been reported as associated with follicles that reach dominance state but do not produce sufficient E2 concentrations capable of stimulating preovulatory LH highs (3, 28), and may probably be also related to prolonged luteal phases. Finally, anovulation by CL persistence was observed, possibly as a result of the emergence of pathologies. In this regard, it has been described that the first ovarian resumption phase usually starts from the first postpartum week in animals with normal calving, but is delayed in those that have suffered dystocic calving, retention of fetal membranes and metabolic diseases that prevent the normal secretion of prostaglandins, maintaining high progesterone levels and allowing the extension of the luteal phase (16). Interestingly in this study, the presentation of dystocia was a factor associated with the delay in the first ovulation (p<0.05) in univariate analysis, however, and probably due to the low frequency of cases, it was not associated in the final model, but it deserves to be considered as a risk factor.

It was also noted that animals with lameness were nine times more likely to show DOR OR=9, CI 95% (1.2-85.2) (p≤0.05); which coincides with previous reports (30, 7). Other pathologies such as mastitis (8), puerperal metritis (16) and dystocia (9) have been associated with the alteration of the reproductive performance of cattle (1). The most possible explanation of this phenomenon has been associated with elevated levels of cytokines, acute-phase proteins and cortisol, which have a negative effect on the timely release of LH and progesterone (31) altering the follicular microenvironment.

The results obtained under the conditions of this study showed that proper body condition during peripartum is a factor that favors early ovulation, while lameness is a risk factor for the occurrence of late ovulation in specialized grazing systems in high tropical areas.

Acknowledgements

To Ganaderia Inversiones Los Sauces Bermudez y Cia. S.C.A., to Dr. Ingrid Guerra, all the personnel of the farms "El Cocli" and "Los Sauces" for their collaboration.

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