Veterinrni Medicin, 60, 2015 (5): 227 234 Originl Pper Effects of seson on plsm progesterone profiles in repet reeding cows M.E. Ghnem 1, M. Nishiori 2 1 Fculty of Veterinry Medicine, Suez Cnl University, Ismili, Egypt 2 Grdute School of Biosphere Science, Hiroshim University, Hiroshim, Jpn ABSTRACT: Forty six Holstein Friesin repet reeding cows (the verge AI/conception ws 5.2 ± 0.2) were investigted using the progesterone ssy fter AI to determine possile differences in plsm progesterone profiles etween summer nd winter sesons. Twenty eight (60.9%) nd 18 (39.1%) cows were followed in summer (June August) nd winter (Decemer Ferury), respectively. In the summer seson, the totl progesterone concentrtions were higher (P < 0.05) in pregnnt cows with norml lutel function compred to those in non-pregnnt nimls with norml lutel function. In contrst, in the winter seson, there ws no difference (P = 0.12) in totl progesterone concentrtions etween pregnnt nd non-pregnnt cows with norml or norml lutel functions. When the progesterone concentrtions were compred, the pregnnt nd non-pregnnt cows with norml lutel functions exhiited no difference (P = 0.92) in summer nd winter sesons. Thus, the present study indictes tht there is no effect of seson on plsm progesterone profiles in repet reeding cows; however in the summer seson, the totl progesterone concentrtions were considerly higher in pregnnt cows with norml lutel function compred to non-pregnnt cows with norml lutel function. Keywords: progesterone; emryonic deth; lutel function; seson; cows Repet-reeder cows re commonly referred to sufertile nimls without ny ntomicl or infectious normlity tht do not ecome pregnnt until the third or susequent reeding or remin infertile fter numerous services. Repet reeding is one of the mjor prolems ffecting reproductive efficiency nd is mjor source of economic wste in diry herds (Brtlett et l. 1986; Cnu et l. 2010; Yusuf et l. 2010). The syndrome contriutes to lower diry profit due to the wstge of semen, insemintion costs, incresing intervls to conception, incresing culling nd replcement costs nd loss of genetic gin through incresed genertion intervls (Brtlett et l. 1986) nd reduced fertility (Grci-Ispierto et l. 2007). Ktgiri nd Tkhshi (2004) stted tht the cuses of infertility in repet reeder cows re usully uncler, ut proly include environmentl, mngement, nd niml fctors. Therefore, it is importnt to identify cuses of repet reeding in order to del with this prolem. The incidence of repet reeding increses in response to indequte oestrus detection (Heuwieser et l. 1997; Pursley et l. 1998), resulting in errors in timing of insemintion in reltion to the onset of stnding oestrus, or insemintion of cows not in oestrus (Yusuf et l. 2010). Other potentil fctors hve lso een suggested, such s qulity of semen nd insemintion technique (Hllp et l. 2006; Morrell 2006), uterine nd/or cervicl/vginl infections (Moss et l. 2002), endocrine disorders (Gustfsson 1998; Bge et l. 2002; Lopez-Gtius et l. 2004), ovultion filures (Kimur et l. 1987; Silvi 1994), ostructed oviducts, defective ov, ntomicl defects of the reproductive trct (Silvi 1994), nd erly emryonic deth (Gustfsson 1998; Bge et l. 2002). Lower prity, norml resumption of postprtum ovrin cycles, nd shorter dys in milk Supported y the Jpnese Society for the Promotion of Science JSPS, (Grnt in-aid No. 18.06222). 227
Originl Pper Veterinrni Medicin, 60, 2015 (5): 227 234 t first AI were identified s risk fctors for repet reeding (Yusuf et l. 2010). Brlett et l. (1986) reported tht there ws no ssocition etween reeding seson nd repet reeding syndrome. However, ovrin folliculr growth nd development of the dominnt follicle cn e ltered during the summer months, nd het stress exerts n inhiitory effect on endocrine function (reduced intensity of oestrus, decresed preovultory LH pek), therey reducing fertility. However, it ws lso oserved tht higher progesterone concentrtions were present in fertile femles during wrm periods. These were ttriuted to incresed ctivity of the CL or the drenls in response to het stress (Gonzlez 1981). Photoperiod length nd temperture vritions re linked to the seson, nd could influence the endocrine regultion of the oestrous cycle. Other fctors such s ody condition t clving, feeding level nd clving to insemintion intervl re lso ffected y the seson, nd cn e modified through mngement prctices (Fulkerson nd Dickens 1985). It hs een demonstrted tht repet reeding syndrome nd infertility increse during summer months (BonDurnt et l. 1991; Gonzlez-Stgnro et l. 1993). Amongst vrious fctors ssocited with the occurrence of repet reeding syndrome, synchronous hormonl interply is one of the mjor fctors cusing fertilistion filure nd erly emryonic mortlity (Kimur et l. 1987; Lfi nd Kneene 1988). Delyed formtion of the corpus luteum (CL) either lone or in comintion with lowered secretion of progesterone during the lutel phse hs een identified s one of the mjor cuses of repet reeding syndrome (Kimur et l. 1987; Thtcher et l. 1994). Informtion relted to sesonl vritions in plsm progesterone nd lutel function in repet reeding nimls is scrce. Therefore, the ojective of the current study ws to investigte the effect of seson on progesterone profiles in pregnnt nd non-pregnnt cows with norml nd norml lutel functions. MATERIAL AND METHODS Animls. This study ws crried out on 46 Holstein Friesin cows t three commercil diry frms in the Hiroshim prefecture in Jpn. Twenty eight (60.9%) nd 18 (39.1%) cows were investigted in summer (June August) nd winter (Decemer Ferury), respectively. The cows were kept in roofed structures with open sides. They were fed totl mixed rtion consisting of lflf, timothy nd ot hy, corn, tofu ground wet, eet pulp, cotton seed nd soyen with pproximtely 17.5% CP nd 73% TDN for lctting cows. Cows were mchine-milked twice dily nd the verge 305 dys milk production ws pproximtely 10 400 kg. A voluntry witing period of 40 dys ws generlly mintined, nd cows detected in oestrus fter this period were rtificilly inseminted. Oestrus detection ws crried out y visul oservtion y the herdsmen. When signs of oestrus were noticed, AI ws performed y experienced technicins. Plsm progesterone profiles. Ten ml of lood were collected from the cows three times/week into heprinised vcuum tues. The lood ws trnsported within 2 h to the lortory in n ice ox nd centrifuged t 1700 g for 15 min. Plsm progesterone concentrtions were determined using doule ntiody enzyme-linked immunosorent ssy s descried (Isoe et l. 2005). The intrssy nd inter-ssy coefficients of vrition were 8.6% nd 12.2%, respectively. The sensitivity of the ssy ws 0.01 ng/ml. Bsed on plsm progesterone profiles, different lutel dysfunctions in repet reeding cows were defined (Kimur et l. 1987; Hommeid et l. 2004; Ghnem et l. 2010). Briefly, norml lutel function ws defined y progesterone concentrtions elevted to 1 ng/ml or more t or efore Dy 6 post-ai nd which reched 2 ng/ml or higher during the mid-lutel phse. Anorml lutel function ws defined s delyed (progesterone concentrtions ws rising to 1 ng/ml fter Dy 6 post-ai) or insufficient (progesterone remined elow 2 ng/ml during the lutel phse) rise in progesterone. Moreover, cow is considered pregnnt when the progesterone concentrtion remined t 2 ng/ml or higher for more thn 42 dys post-ai. On the other hnd, the cow ws considered non-pregnnt when the progesterone concentrtion fell elow 0.5 ng/ml etween Dy 20 nd Dy 42 post-ai (Sntos et l. 2004; Ghnem et l. 2006). In ddition to the determintion of progesterone concentrtions, the cows were plpted per rectum strting four weeks fter AI to confirm the pregnncy. Experimentl design. The cows were distriuted into two min groups (summer nd winter). Within ech group nd sed on the concentrtion 228
Veterinrni Medicin, 60, 2015 (5): 227 234 Originl Pper of progesterone, the nimls were clssified into cows with norml lutel or norml lutel functions. The cows with norml or norml lutel functions were followed, nd then ctegorised s either pregnnt or non-pregnnt cows. Sttisticl nlysis. Dt were nlysed using generl liner models, repeted mesures mixed nlysis of vrince (ANOVA). The dependent continuous vrile ws the progesterone concentrtion in ll nlyses. Anlysis ws done for summer nd winter seprtely, nd then comined together in one nlysis gin to study the sesonl vritions. For seprte nlyses, the first independent fctor ws the time (dys fter insemintion) which hd different repeted mesures levels (e.g. Dy 1, Dy 3, Dy 6), while the second independent fctor ws the condition or tretment type with three levels in summer (pregnnt with norml lutel function, non-pregnnt with norml lutel function nd non-pregnnt with norml lutel function), nd four levels in winter (the three levels s in summer, in ddition to pregnnt with norml lutel function). The time fctor ws used s the withinsujects fctor, while the condition ws used s the etween-sujects fctor. Another nlysis ws done for the effect of seson on progesterone concentrtions together with the time fctor in ll conditions, seprtely. Testing of homogeneity nd sphericity were done using Levene s test for homogeneity of vrinces nd Muchly s test of Sphericity, respectively. The results suggested homogeneity of vrince in most nlyses, while violtion of sphericity due to the lrge numer of level comintions ws oserved. We relied on the Greenhous-Geisser correction for the ssumption of sphericity. The results were discussed s the min effects nd the interction effects of independent fctors on progesterone. Dt of prity, BCS, No. of AI/conception nd clving to lst AI were nlysed using the generl liner model procedure ccording to the three-wy nlysis of vrince (ANOVA). Three independent fctors were studied; seson (summer nd winter), progesterone sttus (norml nd norml lutel functions) nd pregnncy sttus (pregnnt nd non-pregnnt) s min effects together with their interction. Dt were nlysed using SPSS softwre (version 16.0; SPSS Inc., Chicgo, IL, USA) for the min effects, post-hoc tests, followed y the interction effects using Mstt. The results were considered significnt t P 0.05. Tle 1. The effect nd interction of seson, progesterone nd pregnncy sttus on prity, ody condition score nd clving to AI (mens ± SEM) Min nd interction effects Prity BCS Numer of AI/conception Clving to AI (dys) Sesons P = 0.45 P = 0.62 P = 0.63 P = 0.16 Summer 2.5 ± 0.3 3.5 ± 0.1 5.1 ± 0.3 213.5 ± 17.1 Winter 2.0 ± 0.4 3.9 ± 0.2 5.3 ± 0.5 177.8 ± 17.9 Progesterone sttus P = 0.81 P = 0.35 P = 0.24 P = 0.43 Norml lutel function 2.4 ± 0.3 3.5 ± 0.1 5.3 ± 0.3 193.10 ± 12.9 Anorml lutel function 2.4 ± 0.5 3.5 ± 0.2 4.6 ± 0.4 229.4 ± 39.5 Pregnncy sttus P = 0.36 P = 0.09 P = 0.56 P = 0.56 Pregnnt 2.2 ± 0.4 3.5 ± 0.1 5.5 ± 0.3 200.2 ± 13.6 Non-pregnnt 2.5 ± 0.3 3.4 ± 0.1 4.9 ± 0.3 199.7 ± 23.2 Seson * pregnncy sttus * progesterone sttus P = 0.6 P = 0.47 P = 0.87 P = 0.98 Summer pregnnt with norml lutel function 2.5 ± 0.6 3.5 ± 0.1 5.3 ± 0.4 207.8 ± 14.8 Summer non-pregnnt with norml lutel function 2.7 ± 0.5 3.5 ± 0.01 4.9 ± 0.5 189.0 ± 48.0 Summer non-pregnnt with norml lutel function 2.4 ± 0.7 3.6 ± 0.2 5.2 ± 0.4 252.8 ± 52.9 Winter pregnnt with norml lutel function 1.5 ± 0.3 3.7 ± 0.1 5.8 ± 0.5 186.1 ± 28.5 Winter non-pregnnt with norml lutel function 2.4 ± 0.8 3.0 ± 0.3 5.5 ± 1.0 168.8 ± 34.6 Winter non-pregnnt with norml lutel function 2.3 ± 0.6 3.4 ± 0.1 3.7 ± 0.3 171.0 ± 3.9 Within the sme column, mens of the min nd interction effects were non-significnt (P > 0.05), ccording to stndrd 3-wy nlysis of vrince (ANOVA) 229
Originl Pper Veterinrni Medicin, 60, 2015 (5): 227 234 RESULTS Effect nd interction of sesons, progesterone nd pregnncy sttus on prity, ody condition score nd clving to AI in cows Twenty eight cows were investigted in the summer seson (June August) nd 18 cows in the winter seson (Decemer Ferury). The verge prity of the cows, their ody condition score (BCS) t the dy of lst rtificil insemintion, the verge numer of AIs per conception nd the intervl from clving to lst AI re listed in Tle 1. There ws no effect of seson, progesterone or pregnncy sttus on prity, ody condition score, numer of insemintions required for conception nd intervl from clving to AI in repet reeding cows. All P-vlues indicted the non-significnce of min nd interction effects mong these prmeters (Tle 1). Progesterone concentrtions of cows in the summer seson In summer, progesterone concentrtions vried considerly on different dys post-insemintion [F (3.28, 81.86) = 41.37, P = 0.001]. The min effect of the group (pregnnt with norml lutel function, non-pregnnt with norml lutel function nd nonpregnnt with norml lutel function) on the progesterone concentrtion ws significnt, [F (2, 25) = 8.099, P = 0.002]. The time * group interction ws significnt, [F (6.55, 81, 86) = 3.23, P = 0.005], indicting tht the chnges in progesterone concentrtions in the three groups of cows ws differed significntly over time. The totl progesterone concentrtions (ng/ml) were considerly higher (P < 0.05) in pregnnt cows with norml lutel function (2.2 ± 0.2) compred to non-pregnnt cows with norml lutel function (0.9 ± 0.3) throughout the oestrous cycle (Figure 1). Progesterone concentrtions of cows in the winter seson In winter, the differences in progesterone concentrtions mong the four groups (pregnnt with norml lutel function, non-pregnnt with norml lutel function, pregnnt with norml lutel function nd non-pregnnt with norml lutel function) ws non-significnt, lthough mrked difference [F (3.09, 43.38) = 22.76, P = 0.001] ws oserved etween the different time points (dys fter insemintion). The interction of time * group ws lso non-significnt [F (9.30, 43.38) = 1.99, P = 0.06], indicting tht there ws no influence of time on pregnnt nd non-pregnnt cows with norml or norml lutel functions (Figure 2). Progesterone concentrtions of cows in summer nd winter sesons When the progesterone concentrtions in oth sesons were compred to ech other, no difference ws oserved etween the pregnnt nd nonpregnnt cows with norml lutel functions [F (1, 18) = 0.021, P = 0.886], [F (1, 13) = 0.009, P = 0.927]; P4 (ng/ml) 5 4 3 2 1 Pregnnt with norml lutel function Non-pregnnt with norml lutel function Non-pregnnt with norml lutel function d cd c c 0 1 3 6 8 10 13 15 17 20 Dys fter insemintion Figure 1. Progesterone (men ± SEM) concentrtions (ng/ml) in pregnnt cows with norml lutel function, nonpregnnt cows with norml nd norml lutel functions in the summer seson. Letters d, significnt differences mong tretment groups due to interction effect of time * group (P < 0.01) 230
Veterinrni Medicin, 60, 2015 (5): 227 234 Originl Pper 5 4 Pregnnt with norml lutel function Non-pregnnt with norml lutel function Pregnnt with norml lutel function Non-pregnnt with norml lutel function P4 (ng/ml) 3 2 1 0 1 3 6 8 10 13 15 17 20 Dys fter insemintion Figure 2. Progesterone (men ± SEM) concentrtions (ng/ml) in pregnnt cows with norml nd norml lutel functions, non-pregnnt cows with norml nd norml lutel functions in the winter seson moreover, the interction of time * seson ws lso non-significnt [F (3.353, 60.35) = 0.351, P = 0.810], F (2.75, 35.78) = 0.511, P = 0.662], in summer nd winter sesons, respectively. The progesterone concentrtions of non-pregnnt cows with norml lutel functions reveled no difference [F (1, 6) = 1.72, P = 0.237] in summer nd winter sesons. Moreover, the interction of time * seson ws lso non-significnt [F (2.61, 15.64) = 1.15, P = 0.356]. Pregnncy rtes in cows with norml nd norml lutel functions regrdless of the seson Regrdless of the seson, out of 35 cows with norml lutel function, 20 (57.1%) cows ecme pregnnt. Interestingly, out of 11 cows with norml lutel function, three (27.3%) cows ecme pregnnt. DISCUSSION This study ws undertken to clrify the differences in progesterone profiles etween different sesons in repet reeding cttle. In the present study, the numer of repet reeding cows in the frm ws higher in summer thn tht in winter. This might e due to reduced durtion nd intensity of oestrus, ltered folliculr development nd impired emryonic development elicited y het stress (Jordn 2003). The endocrine chnges involved in the decline in folliculr ctivity nd in the ltertion of ovultory function, might led to inferior oocyte nd emryo qulity nd modified uterine environment, therey reducing the likelihood of emryo implnttion (El-Khdrwy et l. 2011). Repet reeding cows were identified sed on the sence of ny other disorders tht could explin the pregnncy filure. Reproductive disorders such s cystic ovries, noestrus nd chronic endometritis increse the risk of pregnncy filure. To void these errors, cows treted for these disorders were not included in the present study. Moreover, wekness of this study ws tht the cows were llocted y seson nd then y progesterone profiles so the resulting numers of cows per group were very limited. This might explin why the progesterone concentrtions in pregnnt nd non-pregnnt cows with norml lutel function exhiited similr profiles without ny significnt differences in oth sesons. Moreover, the progesterone profiles in non-pregnnt cows with norml lutel function were lower in summer compred to winter without reching significnt difference. In similr study, corpus luteum growth nd function were monitored dily for complete oestrous cycle in lctting cyclic Holstein cows in summer nd spring. The length of the lutel phse nd the corpus luteum cross-sectionl re were similr for the two sesonl groups. Serum progesterone secreted etween Dys 6 nd 18 ws lower during summer. Suppressed lutel function might contriute to low fertility when cows re 231
Originl Pper Veterinrni Medicin, 60, 2015 (5): 227 234 inseminted during summer (Howell et l. 1994). However, this issue is controversil; vrious studies hve reported progesterone concentrtions under het stress to e higher, lower, or similr to those under cool conditions (Wolfenson et l. 2000). The divergence mong these findings from the fct tht most short-term, cute experiments did not reproduce the responses otined in long-term, chronic, sesonl studies. In nother study, plsm progesterone levels were significntly higher in winter compred to summer in Holstein cows t 60 to 80 dys postprtum (Wolfenson et l. 2002). No effects of milk yield or prity were detected. Progesterone concentrtions in the erly dys of the cycle were similr in oth sesons; however, during the mid-lutel phse they were 1.5 ng/ml higher in winter compred to summer. Jonsson et l. (1997) reported lower concentrtion of plsm progesterone in cows in summer compred to winter during the development of the second CL fter clving, nd the difference ws not ssocited with ny differences etween sesons, dry mtter intke, ody condition score or milk yield. The ltter indicted tht the decresed progesterone concentrtion in plsm ws directly relted to the het lod nd not necessrily to het stress-induced nutritionl or metolic chnges. The present study indicted tht, in summer, the totl progesterone concentrtions were considerly higher (P < 0.05) in pregnnt cows with norml lutel function thn in non-pregnnt cows with norml lutel function throughout the oestrous cycle. Suoptiml progesterone secretion is possile cuse of low fertility of diry cows during summer het stress (Wolfenson et l. 2000). Interestingly, the totl progesterone concentrtions in pregnnt nd non-pregnnt cows with norml lutel function were similr throughout the oestrous cycle during summer. This is in greement with recent study (Iwzw nd Acost 2013), which suggested tht elevted temperture did not negtively ffect lutel function in cows, nd tht the low fertility oserved during summer ws not due to direct effect of elevted temperture on lutel cells. Dt from the current study support the hypothesis tht the norml lutel phse could ffect the pregnncy rte in repet reeding cows s 57% of cows with norml lutel function ecme pregnnt compred to 27% of cows with norml lutel function, regrdless of the seson. These results re consistent with the findings of Lmming nd Drwsh (1995) who reported tht delyed formtion of the corpus luteum hs mjor effect in terms of emryo survivl nd conception. Kimur et l. (1987) oserved tht 62% of repet reeder cows hd progesterone deficiency during the erly phse of the oestrous cycle. Indequte lutel function my e of prime importnce ecuse norml emryonic development depends upon sequentil chnges in uterine secretion under the influence of progesterone (Wilmut et l. 1986). Lrson et l. (1997) postulted tht delyed onset of the lutel phse could e ssocited with norml emryonic development nd decresed fertility in diry cows. A totl of 37.8% of repet reeding cows displyed typicl ovrin function, ltered progesterone ptterns nd/or ovrin defects negtively impiring fertility (Perez-Mrin nd Espn 2007). Interestingly, pproximtely 43% of the non-pregnnt cows in the present study hd norml lutel function. This finding is consistent with Linres et l. (1982) who reported tht norml emryonic development occurs with norml lutel function. There re other fctors tht cn ffect the function of the CL in cows. Dietry energy restriction my decrese IGF-I concentrtions, cusing ltered folliculr growth nd development of sufunctionl CL (Burns et l. 1997). In ddition, metritis ws le to impir lutel ctivity trnsiently, ut did not seem to hve long-term effect on lutel function (Struve et l. 2013). Moreover, the lutel phse nd the length of the interovultory intervl were oth shorter in heifers with two wves of folliculr development compred to those with three (Ginther et l. 1989). In conclusion, there ws no mrked effect of seson on plsm progesterone profiles in repet reeding cows, lthough the totl progesterone concentrtions were higher in pregnnt cows with norml lutel function compred to non-pregnnt cows with norml lutel function in summer. Dt from the current study support the hypothesis tht n norml lutel phse cn ffect the pregnncy rte in repet reeding cows. Acknowledgement The uthors re thnkful to Dr. N. Isoe (Grdute School of Biosphere Sciences, Hiroshim University), NOSAI Higshi-Hiroshim nd the frmers involved in this study for their coopertion during 232
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