TY - JOUR
AU1 - Thompson, I. M.
AU2 - Tao, S.
AU3 - Branen, J.
AU4 - Ealy, A. D.
AU5 - Dahl, G. E.
AB - ABSTRACT Environmental factors, such as photoperiod and heat stress, can be manipulated during the dry period to influence health, productivity, and reproductive performance of dairy cows in their subsequent lactation. The impacts of photoperiod and heat stress on subsequent lactation are related to alterations in prolactin (PRL) signaling and may affect the expression of pregnancy-specific protein B (PSPB). Additionally, exposure of cows to heat stress during the dry period decreases gestation length; however, the mechanism involved in this process is unknown. The objective of these experiments was to evaluate the influence of environmental factors (i.e., heat stress and photoperiod) during late gestation (i.e., dry period) on PSPB concentrations in plasma of dairy cows. In Exp. 1, cows were dried off in the summer months approximately 46 d before expected calving and assigned randomly to heat stress (HT; n = 30) or cooling (CL; n = 30) treatment. Cooling cows were housed with sprinklers, fans, and shade, whereas HT cows were provided only shade. In Exp. 2, cows were dried off at approximately 60 d before expected calving in summer/fall months and randomly assigned to 3 treatments: long day photoperiod (LDPP: 16L:8D; n = 15), short day photoperiod (SDPP: 8L:16D; n = 14) and SDPP+PRL implant (12 mg/d of PRL at 28 d or 16 mg/d of PRL at 39 d; n = 11). In both experiments, plasma samples were collected at dry off and at −32, −18, −7, −3 and 0 d relative to calving. In Exp. 1, greater concentrations of PSPB were detected in plasma of CL versus HT cows (388.3 ± 24.7 vs. 287.4 ± 23.8 ng/mL; P < 0.01). Concentrations of PSPB did not differ between −46 to −18 d before calving (66.0 ng/mL). However, PSPB concentrations were greater (P < 0.01) for CL cows at d −7 (534.7 > 357.2 ng/mL), −3 (807.2 > 572.2 ng/mL) and 0 (800.8 > 563.5 ng/mL) relative to calving. Additionally, HT cows in Exp. 1 had increased PRL plasma concentrations compared with CL cows (21.01 ± 1.6 vs. 13.78 ± 1.6 ng/mL). In Exp. 2, no differences were detected in plasma concentrations of PSPB (ng/mL) among LDPP, SDPP, or SDPP+PRL groups on d −60 (41.5), −32 (51.7), −18 (58.5), −7 (532.9), −3 (838.2), and 0 (729.4) relative to parturition. Photoperiodic PRL concentrations were 10.81, 7.84, and 4.22 ng/mL for LDPP, SDPP+ PRL, and SDPP, respectively. Results indicate that HT alters PSPB concentrations in late pregnancy, suggesting that placental activity is altered in cows exposed to excessive elevated temperatures around the time of calving. However, the mechanism involved likely is not associated with changes in PRL secretion. INTRODUCTION Environmental factors, such as photoperiod and heat stress, can be manipulated during the dry period to influence performance of dairy cows in their subsequent lactation (Kadzere et al., 2002; Dahl et al., 2011). At least some of the effects of photoperiod and heat stress on subsequent lactation are caused by alterations in prolactin (PRL) concentrations (Auchtung et al., 2005; Tao et al., 2011). Also, cows exposed to heat stress when dry have shorter gestation length (Tao et al., 2011), but the mechanism involved in this acceleration to parturition is unknown. During pregnancy, placental cells migrate and fuse with maternal uterine epithelial cells and deliver secretory products directly into the maternal system. Among the secretory products are the pregnancy associated glycoproteins (PAG), also known as pregnancy-specific protein B (PSPB; Butler et al., 1982). The PSPB is a complex mixture composed of a number of glycosylated and non-glycosylated proteins that can be isolated from early pregnancy. Antibodies raised against PSPB recognize antigenic epitopes specific to placental tissue (Sasser and Ruder, 1987; Sasser et al., 1989). Peripheral concentrations of PSPB (Patel et al., 1995) or bovine PAG (Patel et al., 1997) are correlated to the stage of gestation, number of fetuses, and fetal viability. Not only are PAG in maternal blood being used as a reproductive management tool for early pregnancy diagnosis in cattle (e.g., BioPRYN manufactured by BioTracking LLC Moscow, ID), but they also may be an indicator of embryo/fetal well-being and impending pregnancy loss (Gábor et al., 2007; Thompson et al., 2010). Moreover, increasing concentrations of PAG during gestation and the surge in PAG within 10 d before calving indicate an association with the advance towards parturition. Indeed, there is evidence that PAG is associated with parturition from studies that evaluated changes in PAG responses during late pregnancy by inducing parturition with PGF2α. Animals with normal parturition showed increasing and greater concentrations of PAG as calving approaches. The patterns of plasma PAG were altered in the cases of calving difficulty and stillbirth (Kindahl et al., 2002). We tested the hypothesis that environmental factors that alter PRL secretion during late gestation will influence PSPB concentrations in plasma of dairy cows. MATERIAL AND METHODS Experimental procedures and animal management were approved by the Institutional Animal Care and Use Committee of University of Florida (Exp. 1) and by the University of Illinois Institutional Animal Care and Use Committee (Exp. 2). Experiment 1: Animals and Experimental Design Experiment 1 was conducted over a 2 yr period (2010–2011) at University of Florida Dairy Unit (Hague, FL). Multiparous Holstein cows (n = 60) were dried off approximately 46 d before expected calving during summer months (June, July, August) and assigned randomly to 1 of 2 treatments, heat stress (HT, n = 30) or cooling (CL, n = 30), based on mature equivalent milk production from Dairy Herd Improvement Association (DHIA) records of the previous lactation. Dry cows were housed in a freestall barn with the stall areas for CL cows equipped with a cooling system consisting of shade, sprinklers, and fans, whereas HT cows were provided only shade (see Tao et al. (2011) for details). Fans ran continuously and sprinklers turned on automatically for 1.5 min at 6 min intervals when temperatures exceeded 23.9°C. Photoperiod (14 h light:10 h dark) of the dry cow barn was controlled using metal halide lights, which provided approximately 600 lx intensity at eye level of the cows. The lights were kept on from 0600 to 2000 h. Air temperature and relative humidity of the barn were measured every 15 min by using Hobo Pro Series Temp probes (Onset Computer Corporation, Pocasset, MA). Temperature-humidity index (THI) was calculated based on this equation: THI = (1.8 × T + 32) – [(0.55 − 0.0055 × RH) × (1.8 × Temp − 26)], where Temp = air temperature (°C) and RH = relative humidity (%; Dikmen et al., 2008). Rectal temperature was measured twice daily (0730 and 1430 h) in all dry cows by using a GLA M700 digital thermometer (GLA Agricultural Electronics, San Luis Obispo, CA). The respiratory rate of dry cows was measured thrice weekly (Mon, Wed, Fri) at 1500 h. Experiment 2: Animals and Experimental Design Experiment 2 was conducted over a 2 yr period (2003–2004) at the University of Illinois Dairy (Urbana, IL). Multiparous Holstein cows (n = 40) were dried off approximately 60 d before expected calving during the summer/fall months assigned randomly to 1 of 3 treatments: long day photoperiod (LDPP: 16 h light [16L]:8 h dark [8D]; n = 15), short day photoperiod [SDPP: 8 h light (8L):16 h of dark (16D); n = 14) and SDPP+PRL implant (8L:16D +12 mg/d of PRL starting at 28 d before calving or 8L:16D +16 mg/d of PRL starting at 39 d before calving; n = 11). The different lengths of treatment for the SDPP+PRL group reflect different years of study. Sampling In both experiments, blood samples (8 mL) were collected from coccygeal vessels into sodium-heparinized Vacutainer (Becton Dickinson, Franklin Lakes, NJ) for all the cows at dry off and at –32, –18, –7, –3 and 0 d relative to calving. Samples were immediately put in the ice and centrifuged at 2619 × g at 4°C for 30 min. After centrifugation, the plasma samples were aliquoted and frozen for further analyses. Prolactin was measured according to do Amaral et al. (2009). Pregnancy-Specific Protein B ELISA Assay The commercially available BioPRYN (BioTracking, LLC, Moscow, ID) assay was used for determination of PSPB concentration of the samples. BioPRYN is a typical sandwich ELISA. Rabbit anti-PSPB serum was coated to 96-well micro-titer plates and was used to capture PSPB. The horseradish peroxidase (HRP) labeled anti-PSPB IgG was used to bind to the PSPB that was captured. The development of color occurred with the addition of 3,3',5,5',-Tetramethylbenzidine, the substrate for HRP. Sulfuric acid (1M) was added to stop the reaction and optical density for each well was obtained using a plate reader with a filter wavelength of 450 nm (VersaMax, Molecular Devices, Inc., San Diego, CA). The standard BioPRYN assay provides semiquantitative analysis of samples using 2 standard controls on each plate. To allow for quantitative determination of PSPB in samples, a standard curve of purified PSPB (Butler et al., 1982) was included on each plate. Seven standards (0.125, 0.25, 0.5, 1, 2, 4, and 8 ng/mL) and a blank were used for analysis. A curve was fitted to the standard wells on each plate using a 4-parameter fit using SOFTmax Pro 3.1.1 software (Molecular Devices). The resulting standard curve was used to determine the concentration of PSPB in each sample. Each sample was run twice, once in 2 separate assays. At this stage in gestation, samples required dilution before the assay to bring the concentration of the sample into the range of the standard curve. Samples were either diluted 1:50 or 1:250 in PBS pH 7.2 with 0.5% (wt/vol) BSA. Each sample value is reported as the measured assay concentration times the dilution factor. Two control concentrations (high and low) of PSPB were added to all plates in triplicate to allow for determination of inter- and intra-assay precision for each control concentration. Intra-assay precision for each triplicate control level was determined by dividing the variation of the 3 measurements on a single plate by the mean of the measurements and multiplying by 100 to give a % CV. The intra-assay precision for 8 separate assays was calculated. Inter-assay precision was determined by dividing the SD of the mean of each control concentration from 8 plates by the mean of the means of each control concentration and multiplying by 100 to give a % CV. Intra- and inter-assay precision (% CV) of triplicates (n = 2 × 8) for high concentrations were 2.4 and 5.2%, respectively. Intra- and inter-assay precision (% CV) of triplicates (n = 2 × 8) for low concentrations were 3.1 and 7.3%, respectively. Statistical Analysis In Exp. 1, PROC UNIVARIATE (SAS Inst. Inc., Cary, NC) was used to calculate the THI. Dry period and gestation length for each treatment were analyzed using PROC GLM. Rectal temperature and respiration rate (Exp. 1) and PSPB and PRL (Exp. 1 and 2) responses among treatments were analyzed using repeated measures analyses of the mixed model procedure (PROC MIXED) of SAS. The model included fixed effects of treatment, time, year, and treatment by time with cow (treatment*year) as the random effect. Least squares means were compared using the SLICE function in SAS. RESULTS Experiment 1: Dry Period and Gestation Length, THI, Rectal Temperature, and Respiration Rate Relative to CL cows, the gestation length of HT cows was 4.3 d shorter (P < 0.01; Table 1), which resulted in a 3.9 d reduction (P < 0.01) in dry period length (Table 1). Measurements of THI in the stall areas were similar between HT and CL (77.1 vs. 77.2) cows during the dry period, indicating that both groups of cows were exposed to similar thermal conditions. Additionally, HT cows had greater rectal temperature in the morning (38.8 vs. 38.5°C; P < 0.01; Table 1) and afternoon (39.4 vs. 39.0°C; P < 0.01; Table 1) and greater respiration rates (78.0 vs. 45.6 breaths per min; P < 0.01; Table 1) compared with CL cows. Moreover, CL calves had greater birth weight than HS calves (43.1 vs. 38.3 kg; P < 0.01). Table 1. Dry period length, gestation length, rectal temperatures, and respiration rate of cows exposed to either heat stress (n = 30) or cooling (n = 30) during the dry period Variable  Heat stress  Cooling  P-value  Dry period length, d  36.6 ± 0.98  40.5 ± 0.99  < 0.01  Gestation length, d  272.3 ± 0.96  276.6 ± 0.98  < 0.01  Rectal temperature AM, °C  38.8 ± 0.03  38.5 ± 0.03  < 0.01  Rectal temperature PM, °C  39.4 ± 0.03  39.0 ± 0.03  < 0.01  Respiration rate, breath/min  78.0 ± 1.55  45.6 ± 1.50  < 0.01  Variable  Heat stress  Cooling  P-value  Dry period length, d  36.6 ± 0.98  40.5 ± 0.99  < 0.01  Gestation length, d  272.3 ± 0.96  276.6 ± 0.98  < 0.01  Rectal temperature AM, °C  38.8 ± 0.03  38.5 ± 0.03  < 0.01  Rectal temperature PM, °C  39.4 ± 0.03  39.0 ± 0.03  < 0.01  Respiration rate, breath/min  78.0 ± 1.55  45.6 ± 1.50  < 0.01  View Large Table 1. Dry period length, gestation length, rectal temperatures, and respiration rate of cows exposed to either heat stress (n = 30) or cooling (n = 30) during the dry period Variable  Heat stress  Cooling  P-value  Dry period length, d  36.6 ± 0.98  40.5 ± 0.99  < 0.01  Gestation length, d  272.3 ± 0.96  276.6 ± 0.98  < 0.01  Rectal temperature AM, °C  38.8 ± 0.03  38.5 ± 0.03  < 0.01  Rectal temperature PM, °C  39.4 ± 0.03  39.0 ± 0.03  < 0.01  Respiration rate, breath/min  78.0 ± 1.55  45.6 ± 1.50  < 0.01  Variable  Heat stress  Cooling  P-value  Dry period length, d  36.6 ± 0.98  40.5 ± 0.99  < 0.01  Gestation length, d  272.3 ± 0.96  276.6 ± 0.98  < 0.01  Rectal temperature AM, °C  38.8 ± 0.03  38.5 ± 0.03  < 0.01  Rectal temperature PM, °C  39.4 ± 0.03  39.0 ± 0.03  < 0.01  Respiration rate, breath/min  78.0 ± 1.55  45.6 ± 1.50  < 0.01  View Large Pregnancy-Specific Protein B and Prolactin Concentrations Experiment 1. Greater overall concentrations of PSPB were detected in plasma of CL vs. HT cows (388.3 ± 24.7 vs. 287.4 ± 23.8 ng/mL; P < 0.01; Fig. 1). Concentrations of PSPB did not differ between treatments from d –46 to –18 relative to calving. However, relative to HT cows, PSPB concentrations were greater (P < 0.01) for CL cows at d –7 (534.7 ± 56.5 > 357.2 ± 56.1 ng/mL), –3 (807.2 ± 51.9 > 572.2 ± 49.8 ng/mL), and 0 (800.8 ± 48.0 > 563.5 ± 45.2 ng/mL) relative to calving. Additionally, there were no differences (P = 0.93) in PSPB concentrations associated with the calf gender (male: 333.7 ± 29.7 vs. female: 336.9 ± 22.0 ng/mL). Figure 1. View largeDownload slide Effect of heat stress (n = 30) and cooling (n = 30) during the dry period on pregnancy-specific protein B (PSPB) concentrations during late pregnancy. Cows exposed to cooling during the dry period had greater overall plasma concentrations of PSPB compared with cows in heat stress (388.3 ± 24.7 vs. 287.4 ± 23.8 ng/mL; P < 0.01). Concentrations of PSPB did not differ (P > 0.70) between treatments from d –46 to –18 relative to calving. However, PSPB concentrations were greater (P < 0.01) for cool cows at d –7 (534.7 ± 56.5 > 357.2 ± 56.1 ng/mL), –3 (807.2 ± 51.9 > 572.2 ± 49.8 ng/mL), and 0 (800.8 ± 48.0 > 563.5 ± 45.2 ng/mL) relative to calving. *Means differ from its respective heat stress mean (P < 0.05). Figure 1. View largeDownload slide Effect of heat stress (n = 30) and cooling (n = 30) during the dry period on pregnancy-specific protein B (PSPB) concentrations during late pregnancy. Cows exposed to cooling during the dry period had greater overall plasma concentrations of PSPB compared with cows in heat stress (388.3 ± 24.7 vs. 287.4 ± 23.8 ng/mL; P < 0.01). Concentrations of PSPB did not differ (P > 0.70) between treatments from d –46 to –18 relative to calving. However, PSPB concentrations were greater (P < 0.01) for cool cows at d –7 (534.7 ± 56.5 > 357.2 ± 56.1 ng/mL), –3 (807.2 ± 51.9 > 572.2 ± 49.8 ng/mL), and 0 (800.8 ± 48.0 > 563.5 ± 45.2 ng/mL) relative to calving. *Means differ from its respective heat stress mean (P < 0.05). Plasma PRL concentrations were greater (P < 0.01) for HT cows compared with CL cows (21.01 ± 1.6 vs. 13.78 ± 1.6 ng/mL). Treatment differences were observed throughout the dry period, including the periparturient surge (Tao et al., 2011). Experiment 2. In Exp. 2, no differences were detected in plasma concentrations of PSPB among LDPP, SDPP, or SDPP+PRL groups on d –60 (41.5 ± 26.9 ng/mL), –32 (51.7 ± 26.6 ng/mL), –18 (58.5 ± 26.0 ng/mL), –7 (532.9 ± 39.2 ng/mL), –3 (838.2 ± 48.7 ng/mL), and 0 (729.4 ± 46.3 ng/mL) relative to calving (Fig. 2). Moreover, calf gender did not influence (P = 0.72) the cows PSPB concentrations (male: 384.2 ± 28.0 vs. female: 366.5 ± 45.3 ng/mL). Figure 2. View largeDownload slide Effect of long day photoperiod (LDPP; 16 h of light:8 hours of dark; n = 15), short day photoperiod (SDPP; 8 h of light:16 h of dark; n = 14), and short day photoperiod + prolactin (SDPP+PRL) implant (12 mg/d of prolactin (PRL) starting at 28 d before calving or 16 mg/d of PRL starting at 39 d before calving; n = 11) during the dry period on pregnancy-specific protein B (PSPB) concentrations during late pregnancy. No differences (P > 0.41) were detected in plasma concentrations of PSPB among LDPP, SDPP, or SDPP+PRL groups on d –60 (41.5 ± 26.9 ng/mL), –32 (51.7 ± 26.6 ng/mL), –18 (58.5 ± 26.0 ng/mL), –7 (532.9 ± 39.2 ng/mL), –3 (838.2 ± 48.7 ng/mL), and 0 (729.4 ± 46.3 ng/mL) relative to calving. Figure 2. View largeDownload slide Effect of long day photoperiod (LDPP; 16 h of light:8 hours of dark; n = 15), short day photoperiod (SDPP; 8 h of light:16 h of dark; n = 14), and short day photoperiod + prolactin (SDPP+PRL) implant (12 mg/d of prolactin (PRL) starting at 28 d before calving or 16 mg/d of PRL starting at 39 d before calving; n = 11) during the dry period on pregnancy-specific protein B (PSPB) concentrations during late pregnancy. No differences (P > 0.41) were detected in plasma concentrations of PSPB among LDPP, SDPP, or SDPP+PRL groups on d –60 (41.5 ± 26.9 ng/mL), –32 (51.7 ± 26.6 ng/mL), –18 (58.5 ± 26.0 ng/mL), –7 (532.9 ± 39.2 ng/mL), –3 (838.2 ± 48.7 ng/mL), and 0 (729.4 ± 46.3 ng/mL) relative to calving. Photoperiodic PRL concentrations differed between treatments (P = 0.04) and were 10.81, 7.84, and 4.22 ng/mL for LDPP, SDPP+ PRL, and SDPP, respectively. DISCUSSION The cooling system (fans and sprinklers) used in Exp. 1 was effective in alleviating heat strain on the cows during the dry period. Despite similar barn THI, evidence that heat stress was abated in CL cows was demonstrated by reduced rectal temperature and respiration rate compared with HT cows (do Amaral et al., 2009; Tao et al., 2011). Similar to previous studies (do Amaral et al., 2009, 2011; Tao et al., 2011), HT cows had lighter calf weight, decreased gestation length, and shorter dry period length compared with CL cows. Furthermore, according to previous reports (do Amaral et al., 2011), cows exposed to cooling during the dry period had decreased PRL plasma concentrations compared with HT cows. Results of Exp. 2 were consistent with previous studies which indicated that periparturient PRL concentrations are affected by photoperiod management (Miller et al., 2000; Auchtung et al., 2005; Velasco et al., 2008). Exposure of dry cows to LDPP was associated with greater plasma concentrations of PRL relative to SDPP cows. The replacement of PRL to SDPP cows resulted in an intermediate circulating concentration of PRL relative to LDPP and SDPP cows. The detrimental effects of heat stress during lactation are well documented. Lactating cows exposed to heat stress have compromised reproduction, decreased milk production and immune function, and increased occurrence of postpartum diseases (Hahn, 1997; Kadzere et al., 2002; Collier et al., 2006). Moreover, heat stress during the dry period has carryover effects on the subsequent lactation, dramatically affecting dairy cattle performance. Exposure to dry period heat stress has been associated with decreased subsequent lactation milk yield (do Amaral et al., 2009, 2011; Tao et al., 2011), decreased immune function during the transition period (do Amaral et al., 2010, 2011), altered postpartum hepatic metabolic response (do Amaral et al., 2009), and increased early lactation disease incidence (Thompson et al., 2011). Additionally, cows dried during hot months have increased breeding number, days in milk to first breeding, and days in milk to pregnancy diagnosis in the subsequent lactation compared with cows dried during cool months (Thompson et al., 2011). Dry period heat stress also affects gestation length and calf birth weight (do Amaral et al., 2009, 2011; Tao et al., 2011). In agreement with previous reports, Exp. 1 of the present study showed that relative to HT, CL cows experienced longer gestation length and had calves with greater birth weight. Based on the previous findings, we decided to evaluate the influence of environmental factors (i.e., heat stress and photoperiod) during late gestation on placental/fetal development by measuring plasma PSPB concentrations of dairy cows. Independently of the treatment (i.e., HT or CL), Exp. 1 results agreed with previous reports which showed a steady increase in PSPB/PAG concentrations in late pregnancy (Patel et al., 1997; Green et al., 2005). Differences in PRL concentrations also were detected in Exp. 1. Others also have described an association between PAG and PRL (García-Ispierto et al., 2009). Therefore, Exp. 2 was completed to directly test whether PRL may be controlling PSPB concentrations in late gestation. Results indicate no association between PSPB plasma concentrations and exposure of dry cows to LDPP, SDPP, or SDPP+PRL during late pregnancy. Even though there was an increase in PSPB plasma concentrations from d –60 to d 0 relative to calving, no differences were detected in plasma concentrations of PSPB among LDPP, SDPP, or SDPP+PRL groups on d –60, −32, –18, –7, –3, and 0 relative to calving. As discussed earlier, environmental factors such as heat stress and photoperiod can be manipulated during the dry period and lactation to influence the health and productivity of dairy cows. Several studies have showed that the observed heat stress and photoperiodic effects may alter PRL signaling through an inverse relationship between circulating PRL and PRL receptor (PRL-R) mRNA expression in different tissues. Relative to LDPP, exposure of cows to SDPP decreases circulating PRL concentrations and increases PRL-R gene expression in different tissues including liver, immune cells, and mammary gland (Auchtung et al., 2003, 2004, 2005). Similar to photoperiod, exposure of cows to heat stress during the dry period increases circulating PRL concentrations. Additionally, dry period heat stress is linked to decreases in PRL-R mRNA expression in both hepatic tissue (do Amaral et al., 2009) and lymphocytes (do Amaral et al., 2010). Plasma concentrations of PRL in the present experiments agreed with previous reports. Relative to CL, HT cows had greater PRL plasma concentrations. Moreover, exposure of dry cows to LDPP was correlated with greater PRL concentrations compared with SDPP and SDPP+PRL. Of interest, García-Ispierto et al. (2009) documented that increased PRL plasma concentration in nonaborting Neospora caninum seropositive cows was associated with greater plasma concentrations of PAG-1. In the present study, greater plasma concentrations of PRL in cows exposed to heat stress or LDPP during the dry period was not associated with greater plasma concentrations of PSPB. Despite what previous studies suggest (Auchtung et al., 2003; do Amaral et al., 2010), that photoperiod and heat stress may be influencing physiological responses through PRL signaling was not confirmed in the present study. Changes in late pregnancy placental/fetal development, determined by the measurement of PSPB plasma concentrations of cows exposed to heat stress or different photoperiodic management during the dry period, were not associated with PRL plasma concentrations. In summary, it was observed that HT alters PSPB plasma concentrations in late pregnancy, suggesting that placental activity is compromised in cows exposed to excessive increased temperatures around the time of calving. 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TI - Environmental regulation of pregnancy-specific protein B concentrations during late pregnancy in dairy cattle
JF - Journal of Animal Science
DO - 10.2527/jas.2012-5730
DA - 2013-01-01
UR - https://www.deepdyve.com/lp/oxford-university-press/environmental-regulation-of-pregnancy-specific-protein-b-rRFyf3iVq0
SP - 168
EP - 173
VL - 91
IS - 1
DP - DeepDyve
ER -