Vetrabutine clorhydrate use in dystocic farrowings minimizes hemodynamic sequels in piglets

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Theriogenology 78 (2012) 455– 461 www.theriojournal.com

Vetrabutine clorhydrate use in dystocic farrowings minimizes hemodynamic sequels in piglets M. González-Lozanoa, M.E. Trujillo-Ortegab, M. Alonso-Spilsburyc,*, A.M. Rosalesc, R. Ramírez-Necoecheac, A. González-Macield, R. Martínez-Rodrígueze, M. Becerril-Herreraf, D. Mota-Rojasc a

Postgraduate Division of Animal Science and Health, Faculty of Veterinary and Animal Production, Universidad Nacional Autónoma de México, Mexico b Animal production: swine, Faculty of Veterinary and Animal Production, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico c Universidad Autónoma Metropolitana-Xochimilco, Department of Animal Production and Agriculture, Mexico d Microscopía Electrónica, Instituto Nacional de Pediatría, Mexico e Center for Teaching, Research and Extension in Swine Production. Faculty of Veterinary and Animal Production, Universidad Nacional Autónoma de México f Benemérita Universidad Autónoma de Puebla, PE Ingeniería Agronómica y Zootecnia, Puebla Received 29 January 2011; received in revised form 18 February 2012; accepted 18 February 2012

Abstract The objective was to measure the effects of VC (a uterotonic drug with vasodilator effects) in eutocic and dystocic sows, on the acid– base balance and some vitality traits of piglets at birth. Farrowing was induced with prostaglandin F2␣. Four groups of sows (20 sows/group) were monitored; Groups 1 and 2 were eutocic sows, whereas Groups 3 and 4 were dam-fetal dystocic sows. Groups 1 and 3 (control) were given saline, whereas Groups 2 and 4 were given VC im (1.66 mg/kg of body weight) after the first piglet was born. Piglets’ physio-metabolic performance was monitored peripartum. Treatment with VC reduced (P ⬍ 0.0001) the percentage of intrapartum stillbirths in sows either with eutocic (5.2 vs. 10.0%) and dystocic (7.6 vs. 16.7%) farrowings and increased (P ⬍ 0.0001) the number of pigs born alive without any evidence of AFS (89.9 vs. 79.9%, eutocic and 81.6 vs. 65.2%, dystocic). In addition, for the group of pigs with no acute fetal suffering (AFS), VC treatment enhanced survival responses with a half point grater vitality score in Group 4; it also reduced the latency to first teat contact by 6 min (P ⬍ 0.05) in both treated groups compared to controls; and it improved the condition of the pigs’ umbilical cord, with more adhered (98 vs. 86% in eutocic and 88 vs. 80% in dystocic; P ⬍ 0.05) and less ruptured cords. Moreover, VC reduced the severity of adverse physio-metabolic indicators and the acid– base balance of piglets with AFS at birth by lowering blood lactate (89.8 vs. 93.5 mmol/L in eutocic groups and 94.6 vs. 100.2 mmol/L in dystocic groups; P ⬍ 0.05), PaCO2 and Ca2⫹, and by increasing blood pH, HCO3 and PaO2 levels (P ⬍ 0.05). © 2012 Elsevier Inc. All rights reserved. Keywords: Vetrabutine clorhydrate; Farrowing sow; Uterotonic; Neonatal viability; Dystocia; Blood variables

1. Introduction * Corresponding author. Tel.: ⫹52 55-5483-7004; fax: ⫹52 55-54837004. E-mail address: [email protected] (M. Alonso-Spilsbury). 0093-691X/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.theriogenology.2012.02.025

Parturition is a critical event in polytocous species [1– 4]. In pigs, 3% of sows have maternal dystocia and 35% of farrowings have evidence of fetal suffering [5].

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Sows are of particular interest, since within a litter, acid– base balance of piglets are quite variable [6 –7], representing a degree of either metabolic or respiratory acidosis [8 –12]. Furthermore, alterations of some aspects of acid– base balance (glucose, lactate, pH, PaCO2), as asphyxia indicators, are much more common in newborn piglets born from dystocic farrowings [12]. Although a moderate asphyxia intrapartum is considered normal in all piglets, some have a high degree of asphyxia, due to the cumulative effects of successive contractions and injury or rupture of the umbilical cord [6]. Furthermore, the last piglet born is more likely to be born dead [13,14] or affected by asphyxia. Indeed, there is a relationship between birth assistance and the likelihood of stillbirth due to obstetrical manipulation to correct dystocia [1]. Although oxytocin reduces the duration of farrowing, its use either alone or after prostaglandin-induced parturition has been associated with dystocia and/or higher stillbirth rates in parturient pigs [15,16]. In this regard, dystocia has often not been well managed clinically, since it is not necessary that the sow experiences distress or to wait until many piglets are dead or compromised to confirm the presence of dystocia [17]. More research is needed to identify the primary determinants of stillbirths and thereby reduce the incidence of these losses [18,19]. In that regard, the parity of the sow, farrowing assistance, and animal breed and gender, have been related to perinatal mortality [1,20]. In previous studies, VC, a muscletropic spasmolytic and derivative of papaverine [22] which acts directly on the smooth muscle fibers and has no neurotropic activity, increased the duration of Stage II parturition by 35 min. However, the prevalence of unfavorable outcomes for piglets was reduced in VC-treated sows compared to controls [21,22]. Nevertheless, little attention has been given to examine the influences of VC in sows with eutocia vs. dystocia. Thus, the objective of the present study was to measure the effects of a single dose of VC in eutocic and dystocic sows, on the acid– base balance and some vitality traits of piglets at birth. 2. Materials and methods 2.1. Sows This study was conducted on a commercial pig farm (in Mexico) with approximately 50 farrowings each week. One wk before the expected parturition date, sows were housed in individual crates (with slatted floors) in a farrowing room with the following conditions: an electronic ventilation system, natural lighting

(set at 39.8; Fc ⫺200), average environmental temperature 26 °C, relative humidity of 60%, and no wind. Farrowing was induced with prostaglandin F2␣ (dinoprost tromethamine; Lutalyse, Pharmacia & Upjohn, D. F, Mexico) 24 h before the expected farrowing date, with monitoring started 12 h after treatment. Assistance was provided to all sows during farrowing and piglets at birth; however, obstetrical manipulation was maintained at a minimum, so that farrowing performance data were minimally affected. A total of 80 Yorkshire x Landrace multiparous sows (2nd to 4th parities), were allocated in four groups (20 sows/group); Groups 1 and 2 were eutocic sows, whereas Groups 3 and 4 were dam-fetal dystocic sows. Groups 1 and 3 (control) were given saline (1 mL per 60 kg of live weight), whereas Groups 2 and 4 were treated with 1.66 mg/kg of VC im (Monzal, Boehringer Ingelheim Vetmedica, SA de CV, Guadalajara, Jal, Mexico) after the first piglet was born. All treatments were injected in the neck muscle. According to González-Lozano [17], a maternal-fetal dystocia was considered when at least one of the first four expelled piglets was an intrapartum stillbirths (IPS), because of acute fetal suffering (AFS), or had symptoms of AFS. In addition, dystocic sows had uterine contractions above 30 mm/Hg, compared to ⬍30 mm/Hg from eutocic sows and they also showed uterine atony for at least 40 min, these were monitored with an electronic digital tococardiograph (Fetal Monitor Medical Systems, Inc., CT, USA), farrowings were assisted when the interval between piglets exceeded 40 min. Monitoring was done as described [23,24] in all sows, throughout the second stage of parturition. The uterine transducer was placed with abundant obstetrical gel (Farmacéuticos Altamirano de México, S.A. de C.V., Mexico City) on the abdomen of the sow. Patterns of uterine contractions were recorded on thermal paper. 2.2. Piglets For every farrowing, litter size, piglets born alive and those with IPS were recorded. Stillbirths were classified as ante-partum or intra-partum, based on a complete necropsy examination [21,23,25] conducted within 20 min after expulsion. Preterm neonates were also subjected to a necropsy examination. Bradycardia was defined as fetal heart rate ⬍120 heartbeats per min, and tachycardia when it was ⬎160 heartbeats per min [23]. To quantify the degree of asphyxia that a fetus suffered in utero, fetal heart rate decelerations and AFS were identified and attributed to transitory occlusion of umbilical vessels secondary to uterine contractions, as

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described [26,27]. Piglets with AFS were those that experienced in utero asphyxia (based on fetal electronic monitoring) and survived. They also had the following indicators: some degree of meconium staining in the skin, either hyperglycemia (glucose ⬎85 mg/dL) [6] or hypoglycemia (glucose ⬍50 mg/dL) [28], severe umbilical cord damage (edema, congestion or hemorrhage), lactate ⬎79 mg/dL (lactoacidemia), pCO2 ⬎ 85 mm Hg (hypercapnia), acidemia (blood pH ⬍ 7.2), and low vitality score (⬍6) [29,30]. In the absence of those conditions, piglets were considered born normal. Neonatal vitality was established, using the scale described previously by Zaleski and Hacker [31], and modified by Mota-Rojas, et al. [21]. The latency to first teat contact was also measured. Body temperature of newborn piglets was measured with a tympanic membrane thermometer (ThermoScan Braun, GmbH, Kronburg, Germany), within the first minute of life, together with 1-mL blood samples; immediately after blood sampling, piglets were weighed on a digital scale (Salter Weight-Tronix, Ltd., West Bromwich, UK), and after sampling, they were returned back to their dams, close to the vulva region and latencies to stand on all four feet and to first udder contact were monitored. Umbilical cords were grossly examined at birth and classified as normal (adhered; AUC) or broken (BUC) [26]. 2.2.1. Acid– base imbalance monitoring of newborn piglets Blood samples were placed in glass tubes of 150 ␮L containing lithium heparin. Hematocrit (%), glucose (mg/dL), lactate (mg/dL), electrolytes [Na2⫹, K⫹ and Ca2⫹ (mmol/dL)] and partial pressure of carbon dioxide [PCO2 (mm Hg)] and oxygen [PO2 (mm Hg)] levels, were obtained with an automatic blood gas and electrolyte analyzer (GEM Premier 3000, Instrumentation Laboratory Diagnostics, S.A. de C. V, Mexico).

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2.2. Statistical analyses The four groups of study were analyzed by ANOVA with a General Lineal Model to compare the effect of farrowing type (eutocia or distocia) and the use of VC on the following traits: born alive piglets, IPS, born alive pigs with and without AFS, hemodynamics, individual live weight, latency to contact the teat, body temperature, and glucose, electrolytes and blood gas concentrations. When differences were found, a post hoc Tukey-B test was used to compare means between different combinations of pairs of subgroups: eutocic vs. eutocic with oxytocin, eutocic vs. dystocic, eutocic vs. dystocic with oxytocin, eutocic with oxytocin vs. dystocic, eutocic with oxytocin vs. dystocic with oxytocin, and dystocic vs. dystocic with oxytocin. The frequency of the quality of the umbilical cords was analyzed by a ␹2 test (P ⬍ 0.05), followed by the Fisher’s exact test to locate differences. Since blood pH is a logarithmic scale, the endpoint was analyzed with a Kruskal-Wallis test. The significance level was set for two tails in all cases (P ⬍ 0.05). All statistical analyses were done with SAS Version 9.0. Software [32], and data were provided with means and SEM or ranges. 3. Results In the present study, the type of parturition significantly influenced the performance of sows at farrowing; sows with eutocia had better performance [more born alive piglets and normal (born alive without AFS) and lower number of IPS and live with AFS], compared with sows experiencing dystocia (Table 1). Treatment with VC reduced the frequency of IPS in sows with dystocic farrowings (P ⬍ 0.0001). Furthermore, the number of pigs born alive without evidence of AFS (normal) was greater (P ⬍ 0.0001) in sows treated with VC, compared with the control groups (Table 1).

Table 1 Effects of VC on farrowing sow performance, according to the farrowing type.

Number of sows Born alive piglets (no. [%)]) Intra-partum stillbirths [no. (%)] Ante-partum stillbirths [no. (%)] Born alive with acute fetal suffering [no. (%)] Born alive, without acute fetal suffering [no. (%)] Total born

Group 1 Eutocic

Group 2 Eutocic ⫹ VC

Group 3 Dystocic

Group 4 Dystocic ⫹ VC

20 202 (88.2)a 23 (10.0) 4 (1.7) 20 (8.7)a 182 (79.9)b

20 213 (93.4)a 12 (5.3)a 3 (1.3) 8 (3.2)a 205 (89.9)c

20 187 (82.4)b 38 (16.7)b 2 (0.9) 39 (17.2)b 148 (65.2)a

20 203 (91.0)a 17 (7.6)a 3 (1.3) 21 (9.4)a 182 (81.6)b

229

228

227

223c

within a row, numbers (or proportions) without a common superscript differed (P ⬍ 0.0001).

a– c

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Table 2 Physio-metabolic performance from piglets with no acute fetal suffering from sows (in two farrowing conditions) treated with VC.

Vitality (median ⫾ range) Umbilical cord [A: B] (no.)* Latency to contact the teat (min) Body temperature (°C) Glucose (mg/dL) Lactate (mg/dL) pH (median ⫾ range)** HCO3- (mmol/L) PaO2 (mm Hg) PaCO2 (mm Hg) Ca2⫹ (mmol/L)

Group 1 Eutocic

Group 2 Eutocic ⫹ VC

Group 3 Dystocic

Group 4 Dystocic ⫹ VC

9 (7–10) 156:26 29.7 ⫾ 9.1 37.6 ⫾ 0.5 63.5 ⫾ 6.4 42.2 ⫾ 11.9 7.2 (6.7–7.7) 20.9 ⫾ 2.5 25.5 ⫾ 5.4 51.2 ⫾ 8.6 1.69 ⫾ 0.1

9 (8–10)a 201a:4a 22.9 ⫾ 5.5a 37.9 ⫾ 0.7a 70.8 ⫾ 15.7a 34.3 ⫾ 4.3a 7.3 (6.8–7.9)a 23.1 ⫾ 2.4a 28.2 ⫾ 5.9a 47.1 ⫾ 9.3a 1.55 ⫾ 0.2a

8 (5–10)bd 118d:30d 30.1 ⫾ 11.1d 37.6 ⫾ 0.7d 64.5 ⫾ 8.7d 40.9 ⫾ 8.3d 7.2 (6.7–7.7)d 22.1 ⫾ 2.4bd 25.9 ⫾ 6.8d 54.6 ⫾ 8.7bd 1. ⫾ 0.2d

8.5 (5–10)ef 161ef: 21ef 24.6 ⫾ 6.5cf 37.5 ⫾ 0.7e 67.8 ⫾ 12.7cf 36.6 ⫾ 5.5cef 7.2 (6.8–7.8)cef 22.4 ⫾ 2.1ce 27.3 ⫾ 6.6c 50.9 ⫾ 8.8ef 1.57 ⫾ 0.2c f

Values with different superscripts differ between different combination of pairs of subgroups (P ⬍ 0.05). A, adhered; B, broken. a–f

Piglets born by eutocia (Table 2), had better vitality scores and the values of HCO3 and PaCO2 were more favorable compared with those pigs from dystocic sows (P ⬍ 0.05). Furthermore, metabolic endpoints were better for piglets born from sows treated with VC (greater concentrations of oxygen, blood glucose, pH values and lower concentrations of CO2 and lactate), regardless of the type of farrowing. Although all piglets included in this group were born without any evidence of AFS, VC treatment positively improved the proportion of adhered umbilical cords (45 and 43 more AUC for eutocic and dystocic, respectively, P ⬍ 0.05) and reduced the time to make teat contact (⬃6 min less, P ⬍ 0.05). There were no significant differences among groups for blood concentrations of Na2⫹ and K⫹. Values for physio-metabolic parameters in piglets with AFS are shown (Table 3). Even when all piglets were allocated to an AFS group, there was a positive effect of the treatment with VC on some survival traits

of the piglets born, regardless of the type of parturition [higher vitality, less incidence of BUC and approximately 16 and 9 min less time to contact the teat (P ⬍ 0.05)]. The only metabolic traits favorable for piglets included in this classification (AFS) were the pH, HCO3 and PaO2 for those born from eutocic farrowings, and pH, HCO3 and Ca2⫹for those born from dystocia, exclusively from sows given VC. There were no significant differences among groups for the following traits: body temperature, glucose, and Na2⫹ and K⫹ concentrations. 4. Discussion 4.1. Type of parturition The results of this study confirmed prior observations that asphyxia indicators were significantly more evident in piglets born from dystocic sows [5]. Never-

Table 3 Physio-metabolic performance from piglets with acute fetal suffering from sows treated with vetrabutine clorhydrate in different farrowing conditions.

Vitality (median ⫾ range) Umbilical cord [A: B] (no.)* Latency to contact the teat (min) Lactate (mg/dL) pH (median ⫾ range)** HCO3- (mmol/L) PaO2 (mm Hg) PaCO2 (mm Hg) Ca2⫹ (mmol/L) a– e

Group 1 Eutocic

Group 2 Eutocic ⫹ VC

Group 3 Dystocic

Group 4 Dystocic ⫹ VC

5 (3–7) 0:20 54.7 ⫾ 5.2 93.5 ⫾ 6.2 7.1 (6.7–7.5) 17.84 ⫾ 1.2 18.75 ⫾ 2.3 96.05 ⫾ 20.4 1.96 ⫾ 0.1

6 (4–8)a 3a:5a 37.8 ⫾ 4.5a 89.8 ⫾ 4.9 7.2 (7.0–7.3) 21.73 ⫾ 1.5a 23.25 ⫾ 4.5a 88.25 ⫾ 3.2 1.87 ⫾ 0.0

5 (3–7)d 0d:39d 56.9 ⫾ 8.9d 100.2 ⫾ 13.1d 7.0 (6.7–7.3)d 17.67 ⫾ 1.3d 16.88 ⫾ 3.4d 101.07 ⫾ 8.9d 2.01 ⫾ 0.2d

6 (3–9)cf 5cf: 16cf 47.7 ⫾ 6.2cef 94.6 ⫾ 7.9 7.1 (6.7–7.5)e 20.44 ⫾ 2.2cf 20.70 ⫾ 6.1 91.61 ⫾ 6.3 1.89 ⫾ 0.1e

Values with different superscripts differ between different combination of pairs of subgroups (P ⬍ 0.05).

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theless, in the present study, the use of VC had positive outcomes when sows with maternal-fetal dystocia (reduced IPS and AFS) were treated. In a previous study [22], using VC in eutocic farrowings, uterine activity was significantly lower than in the control group, indicating that VC had a suppressive effect on the uterine contractions of the sow at parturition. It is known that these contractions slow down placental blood flow [33], and therefore reduce oxygen supply to the fetus. The accumulation of successive uterine contractions increases the risk of acid– base imbalance, where below normal values any additional effect (e.g., occlusion, damage or even rupture of the umbilical cord) is decisive, triggering severe asphyxia at birth [34]. The modulation of the uterine contractions produced by VC [22] may explain the lower number of adverse effects observed in newly born piglets from the dystocic farrowings found in this study. Furthermore, hemo-dynamic variables and gases in piglets and litter performance in sows with both types of parturition were noteworthy. 4.2. Piglet vitality and latency to contact dams’ teat Vitality of all born piglets was enhanced and latency contacting the dams’ udder was reduced using VC, regardless of birth conditions (with or without AFS). According to Casellas, et al. [35], piglets with high vitality scores can reach the teat and start suckling faster than those with low vitality, consistent with our results. Conversely, it is noteworthy that newborn piglets receive unusually low maternity care from their dams. 4.3. Perinatal effects of acute fetal suffering Treatment with VC had a positive effect on the performance and metabolic acid– base balance of piglets born from either eutocic or dystocic sows. Furthermore, VC treatment increased the number of born alive without AFS in both farrowing type groups. For the acute fetal suffering group, the effects of VC favored the following metabolic traits: pH, HCO3 and PaO2 for the eutocic ones, and pH, HCO3 and Ca2⫹for those from dystocic farrowings. However, lactate and PCO2 remained high in all cases for the AFS group, clearly indicating metabolic and respiratory acidosis. The degree of acidosis is considered an important factor determining neonatal performance [36,37]. In human babies, metabolic acidosis results from excessive formation of metabolic acids (e.g., lactate and subsequent accumulation during a hypoxemic period; moreover, it causes complications in newborns [36]). Normally, CO2 elimination (and therefore carbonic

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acid), and lactate in fetal blood depend almost entirely on the placenta, helping to compensate the deficit of fetal oxygen [38]. If the placental blood supply is affected or diminished, hypoxemia develops rapidly, resulting in an anaerobic metabolism and lactate production [17]. Previously, it has been shown that the effect of uterine contractions has detrimental consequences on the acid– base balance; nevertheless, consequences due to the farrowing type and the modifications of placenta metabolism level on the piglets’ conditions at birth need to be considered. One advantage that a newborn has is that the affinity of O2 in blood is higher than in the sow [39], which compensates for some deficiencies. The uterus-placenta tissue may be the origin of lactate raise in the swine umbilical flow; these tissues produce lactate, which is released into the umbilical and uterine flow in other domestic species [40]. In this study, there was a dramatic positive effect on survival traits of piglets born from sows treated with VC, regardless of the type of farrowing (high vitality, lower BUC frequency and less time to contact the teat). In this regard, piglets born with broken umbilical cords had significantly lower pH levels at birth, compared with those born with intact umbilical cords [8]. In addition, asphyxiated newborns typically have other complications, including hemostatic and cardiovascular dysfunctions [41]. In the present study, since metabolic measures were done right at birth, they only reflect disturbances of acid– base imbalance because of intrauterine events and/or the expulsion process of the piglets [8]. In conclusion, VC treatment resulted in a lower frequency of IPS piglets and those born with AFS in sows with or without dystocia. Also, the use of the uterotonic drug with vasodilator effects diminished the severity of adverse outcomes on the metabolic indicators and the acid– base balance of the piglets at birth, and enhanced survival responses (major vitality and less time to udder contact and to suckle colostrum) as well as the physical state of the umbilical cord. It was clear that the type of parturition dramatically influenced the litter performance of farrowing sows, so that indicators from sows that went through eutocic process were better compared with those of sows suffering dystocia. A similar effect was observed in the survival traits and blood metabolites. Indeed, VC treatment in the dystocic group had similar outcome relative to those of normal eutocic farrowings without VC administration. The findings have important implications for man-

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agement of farrowing sows and provide a means to improve piglet survival. [11]

Acknowledgments Miguel González-Lozano is a member of the program of Doctorado en Ciencias de la Producción y de la Salud Animal, UNAM, and was supported by the scholarship Number 168246 from CONACYT, Mexico. Daniel Mota-Rojas, María Alonso-Spilsbury, Ana María Rosales-Torres, María Elena Trujillo-Ortega and Ramiro Ramírez Necoechea were supported as members, by the SNI (Mexico). References [1] Canario L, Roy N, Gruand J, Bidanel JP. Genetic variation of farrowing kinetics traits and their relationships with litter size and perinatal mortality in French Large White sows. J Anim Sci 2006;84:1053– 8. [2] Olmos-Hernandez A, Trujillo-Ortega ME, Alonso-Spilsbury M, Sanchez-Aparicio P, Ramirez-Necoechea R, Mota-Rojas A. Foetal monitoring, uterine dynamics and reproductive performance in spontaneous farrowings in sows. J Appl Anim Res 2008;33:181–5. [3] Sanchez-Aparicio P, Mota-Rojas D, Nava-Ocampo AA, Trujillo-Ortega ME, Alfaro-Rodriguez A, Arch E, Alonso-Spilsbury M. Effects of sildenafil on the fetal growth of guinea pigs and their ability to survive induced intrapartum asphyxia. Am J Obstet Gynecol 2008;198:127. [4] Sanchez-Aparicio P, Mota-Rojas D, Trujillo-Ortega ME, ZarcoQuintero LA, Becerril-Herrera M, Alonso-Spilsbury M, AlfaroRodriguez A. Effect of prostaglandins for inducing birth on weight, vitality and physiological response in newborn pigs. J Appl Anim Res 2009;36:113– 8. [5] Gonzalez-Lozano M, Mota-Rojas D, Velazquez-Armenta EY, Nava-Ocampo AA, Hernandez-Gonzalez R, Becerril-Herrera M, Trujillo-Ortega ME, Alonso-Spilsbury M. Obstetric and fetal outcomes in dystocic and eutocic sows to an injection of exogenous oxytocin during farrowing. Can Vet J 2009;50: 1273–7. [6] Herpin P, LeDividich J, Hulin JC, Fillaut M, DeMarco F, Bertin R. Effect of the level of asphyxia during delivery on viability at birth and early postnatal vitality of newborn pigs. J Anim Sci 1996;74:2067–75. [7] Chiang FE, Rodway RG. Determinations of umbilical cord beta-endorphin concentration and blood gas parameters in newborn piglets. Res Vet Sci 1997;63:107–11. [8] van Dijk AJ, van der Lende T, Taverne MAM. Acid-base balance of umbilical artery blood of liveborn piglets at birth and its relation with factors affecting delivery of individual piglets. Theriogenology 2006;66:1824 –33. [9] Orozco-Gregorio H, Mota-Rojas D, Bonilla-Jaime H, TrujilloOrtega ME, Becerril-Herrera M, Hernandez-Gonzalez R, Villanueva-Garcia D. Effects of administration of caffeine on metabolic variables in neonatal pigs with peripartum asphyxia. Am J Vet Res 2010;71:1214 –9. [10] Crissiuma AL, Juppa CJ, de Almeida FM, Gershony LC, Labarthe NV. Influence of the order of birth on blood gasometry

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