Derar Refaat Ibraheem Mohammad a,b, Mootaz Ahmad Mohammad Abdel-Rahman b RESEARCH. Introduction

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1 Journal of Veterinary Behavior (2013) 8, RESEARCH A comparative study on behavioral, physiological, and adrenal changes in buffaloes during the first stage of labor with normal and difficult parturition Derar Refaat Ibraheem Mohammad a,b, Mootaz Ahmad Mohammad Abdel-Rahman b a Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt; and b Department of Animal Hygiene, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt. KEYWORDS: buffaloes; dystocia; behavior; physiology; adrenal Abstract The present study was primarily carried out to trace the behavioral, physiological, and adrenal changes during the first stage of labor in cases of dystocia, either in parturient buffalo heifers or cows, and their clinical significance. Of the 118 investigated buffalo herds, 40 cows (dystocia 5 20 and eutocia 5 20) and 40 heifers (dystocia 5 20 and eutocia 5 20) were used in this study. Cows approaching actual birth were transferred to a calving box with straw bedding. Behavior of the studied animals was recorded from the time that the animal was moved to the calving box until the emergence of the fetal limbs in the vulval lips. If no progress in parturition was observed within two hours after the rupture of fetal sacs (end of the first stage), these cases were considered as suffering dystocia. As the fetal limbs emerged from the birth canal, animals were examined clinically to determine their average pulse and respiratory rates as well as body temperature. Blood samples were collected to determine the cow/heifers cortisol level. Results of the present study indicated that dystocia was accompanied by disturbed physiological status and cortisol levels. Practical monitoring system of parturient animals, through observing behavioral, physiological, and adrenal aspects during calving, should be regarded to expect dystocia and provide help for the animal in the appropriate time. Ó 2013 Elsevier Inc. All rights reserved. Introduction The birth of a healthy calf is one of the main basic requirements for the economic efficiency in cattle and buffalo production. The onset of labor in the standing buffalo heifer or cow is marked by extending of the tail of the animal, bending of the hip joint, and straddling of the Address for reprints requests and correspondence: Derar Refaat Ibraheem Mohammad, PhD, Department of Theriogenology, Faculty of Veterinary Medicine, Assiut University, Assiut, Egypt. Tel: ; Fax: hind legs. In the lying position, there is also stretching of the neck and limbs (Fischer and Bodhipashka, 1992). The first stage of calving starts with irregular, intermittent, and uncoordinated contractions of uterine muscles (Tulloch, 1992). When the uterine contraction becomes intense and regular, the animal attempts to push the fetus out of the uterus. The water bag appears at the vulval lips and subsequently ruptures, and the allantoic fluids flow from the vulva. The fetus and amniotic fluids flow through the cervix and vagina (Hafez, 1992). Calves from difficult parturition show a clearly increased mortality during the first 24 hours after parturition (Patterson et al., 1987; Wittum et al., 1993; Nix et al., 1998). Therefore, it is of /$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. doi: /j.jveb

2 Mohammad and Abdel-Rahman Behavioral, physiological, and adrenal changes in parturient buffaloes 47 particular interest to detect difficulties during parturition as early as possible. Parturition process is divided into three phases. The first stage of labor begins with the dilatation of the cervix and ends with the rupture of the chorioallantois in the vagina (Jackson, 1995). In the second stage of labor, the calf is visible in the rime vulvae and is expelled, followed by the fetal membranes in the third stage. Parturient behavior in most animals during the first stage of parturition begins with exploration of the parturient box along with an extensive olfactory check of the ground, and pushing straw with their heads and front limbs to form a resting place. As the first stage of parturition advances, most parturient animals lie down and get up several times, scraping the floor, looking back at the abdomen. Rupture of the fetal sac leads to apparent relief, and some parturient animals begin to lick up the escaped amniotic fluids (Wehrend et al., 2006). In fact, earlier studies have reported on the behavior of parturient cows and heifers during the antepartal period and the expulsion phase (Dufty, 1971; O Mary and Hillers, 1976; Kharche et al., 1982; Berglund et al., 1987; Mukasa and Mattoni, 1990; Wehrend et al., 2005); however, there are hardly any studies, especially on buffaloes, about their behavior during the first stage of labor. As the incidence of dystocia among buffalo herds is high, and therefore the mortality rate of the delivered calves is also high, the aim of the present study is to observe the behavioral, physiological, and adrenal changes of buffalo cows and heifers during the first stage of labor, and how to use these changes as a sign of a calving problem during parturition so that it can be resolved as early as possible. Materials and methods Animals used and management Eighty parturient buffalo cows and heifers of 118 members of investigated herds were used in this study during their first stage of parturition (20 heifers with eutocia, 20 heifers with dystocia, 20 multiparous cows with eutocia, and 20 multiparous cows with dystocia). The average age of the heifers and cows at the time of parturition was 3 and 7 years, respectively. Animals in the present study were targeted using the Ovsynch program and fixed time insemination. The expected time of parturition was well defined from records. Twenty animals in each group were targeted for better comparison and analysis. Each animal was separated from the herd one week before expected parturition and kept in a separate well-ventilated and well-lit house with freely available water and food. All separated animals were checked continuously for externally visible signs of parturition. Cows and heifers in the first stage of parturition (edematous vulva, relaxation of pelvic ligaments, leakage of colostrum from the teats, and appearance of the amniotic sac in the cervix through vaginal examination) were transferred to a calving box with straw bedding. Behavioral observations Behavior of the experimented animals was recorded and analyzed according to Wehrend et al. (2006). The parturient animal was observed from a distance of 5 m outside the calving box starting from the time that the animal was moved to the calving box until the emergence of the fetal limbs from the vulval lips. The recorded behavior was analyzed as follows: - Exploratory behavior, degree of restlessness (degree 1: calm, degree 2: restless with frequent change of activities, degree 3: very restless with permanent interruption in case of slight environmental stimuli), lying down and getting up, scraping on the floor with the forefeet, pawing, ingestion of the amniotic fluid, looking back at the abdomen, hunching of the back, vocalization, grooming, and rubbing against the wall. If no progress in parturition was observed for two hours after the fetal sacs had ruptured (end of the first stage), a vaginal examination was carried out, and these cases were considered as dystocia (the normal duration of the second stage or the fetal expulsion stage is minutes according to Senger, 2003) if the living calf could be pulled out after correction of its position and posture. Physiological measurements With the emergence of the fetal limbs from the rima vulvae, the cow/heifers were examined clinically to determine their average pulse rate, respiratory rate, and body temperature, according to Blood and Henderson (1974) and Blood and Radostits (1990). Blood sampling and analysis With the emergence of the fetal limbs, blood samples also were collected from the jugular vein of the cow/ heifers. Samples were allowed to coagulate at room temperature, and serum was separated by centrifugation. The sera were frozen at 220 C until further analysis to determine the cow/heifers cortisol level using the TDx FLx system with fluorescence polarization and the competitive binding technique according to Dandliker and Feigen (1970) and Dandliker and Saussure (1973). Statistical analysis Statistical analysis of the collected data was carried out according to the procedures of completely random design (SAS, 1995). Results Results are presented in Tables 1 5 and Figure 1. Both pulse and respiratory rates of heifers and cows were significantly increased during the first stage of parturition with

3 48 Journal of Veterinary Behavior, Vol 8, No 1, January/February 2013 Table 1 Behavioral pattern of buffalo heifers during the first stage of labor with eutocia or dystocia Parameter Eutocia Dystocia n % n % P Value Exploratory behavior NS Restlessness Degree 1: calm ,0.01 Degree 2: restless NS Degree 3: very restless ,0.01 Lying down and getting up NS Scraping on the floor NS Pawing ,0.01 Ingestion of amniotic fluid NS Looking back at the abdomen ,0.01 Hunching of the back ,0.01 Vocalization NS Grooming NS Rubbing against the wall NS dystocia compared with eutocia, but their measured rectal temperatures were not significantly affected. The behavioral pattern did not differ significantly between buffalo heifers and cows regardless of the incidence of dystocia. However, vocalization was predominantly more frequent (P, 0.05) in heifers (in both the eutocia and dystocia groups) than in cows. Although nonsignificant, ingestion of amniotic fluid was more prominent in heifers than in cows (P, 0.09). In both heifers and cows, higher percentages of pawing, looking back to the flank, hunching the back, and higher levels of restlessness were observed in the dystocia groups compared with the eutocia groups (P, 0.01). Generally, the first stage of labor was significantly longer in heifers than in cows and in both heifers Table 2 Behavioral pattern of buffalo cows during the first stage of labor with eutocia or dystocia Parameter Eutocia Dystocia n % n % P Value Exploratory behavior NS Restlessness Degree 1: calm ,0.01 Degree 2: restless NS Degree 3: very restless ,0.01 Lying down and getting up NS Scraping on the floor NS Pawing ,0.01 Ingestion of amniotic fluid NS Looking back at the abdomen ,0.01 Hunching of the back ,0.01 Vocalization NS Grooming NS Rubbing against the wall NS Table 3 Health status measurements of buffalo heifers at the end of the first stage of labor with eutocia or dystocia Parameter Eutocia Dystocia P Value Duration (hours) ,0.01 Pulse rate (no./min) ,0.01 Respiratory rate (no./min) ,0.01 Body temperature ( C) NS NS, nonsignificant. and cows suffering from dystocia compared with spontaneous calving. Cortisol level during the first stage of parturition was significantly higher in the serum of parturient animals suffering from dystocia (P, 0.01). Discussion Studying an animal s behavior plays an important role in measuring its welfare. As the incidence of dystocia among buffalo herds is high, and thus the mortality rate of the delivered calves is also high, studying the parturient behavioral pattern of buffalo cows and heifers during the first stage of labor is important because the changes of this pattern can be used as a sign of impending dystocia. The finding of this study indicated that, as a result of the exaggerated behavioral pattern, most of the heifers and cows that suffered from dystocia showed prominent disturbances in their parturient behavioral pattern, especially restlessness, pawing the floor, looking back at the abdomen, and hunching the back. In the present study, the first stage of labor was significantly longer in heifers than in cows. Moreover, dystocia lengthened the duration of the first stage of labor beyond the norm. The first stage of labor in buffaloes takes minutes (Tulloch, 1988) or minutes (Andrabi and Gill, 1993). Jainudeen and Hafez (1992) reported that the first stage of labor lasts 1-2 hours, and is longer in primiparous than in pluriparous buffaloes. Heifers were more affected by the stress of calving than cows and showed a nonsignificant increase in the percentage of restless, pawing, vocalizing, and amniotic fluid-ingesting animals. Additional evidence supporting these findings was that the mean cortisol level was higher in heifers than in cows, indicating that heifers responded more acutely to the stress of parturition or dystocia. The behavioral differences between cows and heifers with eutocia, such as Table 4 Health status measurements of buffalo cows at the end of the first stage of labor with eutocia or dystocia Parameter Eutocia Dystocia P Value Duration (hours) ,0.01 Pulse rate (no./min) ,0.01 Respiratory rate (no./min) ,0.01 Body temperature ( C) NS

4 Mohammad and Abdel-Rahman Behavioral, physiological, and adrenal changes in parturient buffaloes 49 Table 5 Average serum cortisol level (mg/100 ml) of buffalo heifers and cows at the end of the first stage of labor with eutocia or dystocia the higher proportion of heifers that showed pawing with the forefeet and restlessness during the first stage of labor, should not be misconstrued as signs of dystocia. These differences in behavioral patterns between cows and heifers might explain why obstetric intervention is more frequent in heifers than in cows (Dargartz et al., 2004). The comparative assessment of the behavior of cows with eutocia and dystocia showed significant differences in 4 of 11 behavioral parameters studied here. More cows with dystocia showed restlessness, pawing, looking back at the flank, and hunching the back. These parameters can be assessed as signs of pain and should be included in a monitoring system. The observation of these behavioral elements should highlight the possibility that there may be a problem in the first stage of labor. These findings were in agreement with those of Kharche et al. (1982), Mukasa and Mattoni (1990), Dargartz et al. (2004), and Wehrend et al. (2006). These parameters can be assessed as signs of pain and should be included in the practical monitoring system of parturient animals. However, the observation of these behavioral elements should highlight the possibility of a problem during the first stage of labor, and thus be considered so that the necessary precautions and solutions to help and save the lives of both the mother and the living calf can be implemented. The data collected during the present study showed the effect of parturition on pulse rate, respiratory rate, and body temperature of the investigated animals. These results revealed that both the pulse and respiratory rates of heifers and cows were significantly increased during the first stage µg / 100 ml Item Eutocia Dystocia P Value Heifers ,0.01 Cows , Eutocia Dystocia 0 Heifers Cows Figure 1 Serum cortisol level of heifers and cows during first stage of labor with eutocia or dystocia. of parturition in those with dystocia compared with eutocia; however, their measured rectal temperatures were not significantly affected. This finding indicated that parturition was accompanied with physiological disturbances that were more prominent during dystocia than eutocia as a result of changes in the animal s body to meet the more stressful situation of dystocia (Banerjee, 1982; Berglunmd et al., 1987; Radostits et al., 1994). The data represented in the present study illustrated that the cortisol level during the first stage of parturition was significantly higher in the serum of parturient animals suffering from dystocia. The significant increase in the blood cortisol level of parturient heifers and cows that suffered from dystocia indicated an incidence of a powerful acute stress due to this condition followed by an outpouring of adrenocorticotrophic hormone, which in turn caused the adrenal cortex to increase its secretion of glucocorticoids, including cortisol (McDonald, 1969; Burchfield et al., 1980; Stephens, 1981; Kindahl et al., 2002). However, the elevated cortisol level was obvious in heifers carrying their first pregnancy with less experience in testing this situation compared with (although nonsignificant difference) multiparous buffalo cows more accustomed to such situations. It was indicated that cows induced to deliver their fetus using corticosteroids more frequently suffered from difficult parturition than control normally delivered cows (Ball and Peters, 2004). In buffaloes, the gradual increase in plasma cortisol concentration during the prepartum period peaked on the day of calving and could be explained by prepartum anxiety and myometrial contractions associated with the stress of parturition (Sathya et al., 2005). Furthermore, parturition is an inflammatory process involving the release of cytokines and prostaglandins, which stimulate the hypophyseal adrenal axis (Rivest, 2001). Therefore, the increase in plasma cortisol concentrations during the immediate prepartum period could also be related to increasing concentrations of inflammatory mediators. In conclusion, the first stage of labor in parturient buffalo heifers and cows suffering from dystocia was accompanied with more obvious changes in their behavioral, physiological, and adrenal parameters. These changes can be assessed as signs of more pain and more stressful conditions and should be included in the practical monitoring of parturient animals to highlight the possibility of a problem during labor, and so that the necessary precautions and solutions can be taken to help save the lives of both the mother and the living calf. References Andrabi, S.Z.A., Gill, R.S., Studies on calving in buffaloes. Indian J. Anim. Prod. Manag. 9, Ball, P.J.H., Peters, A.R., Reproduction in Cattle, 3rd Ed. Blackwell Publishing Ltd, Oxford, UK, pp Banerjee, S., A Textbook of Animal Husbandry, 5th Ed. Oxford and IBH Publishing Company, New Delhi, India, pp

5 50 Journal of Veterinary Behavior, Vol 8, No 1, January/February 2013 Berglund, B., Philipson, I., Danell, O., External signs of preparation for calving on course of parturition in Swedish dairy cattle. Anim. Reprod. Sci. 15, Blood, D.C., Henderson, J.A., Veterinary Medicine, 4th Ed. Bailliere Tindall, London, UK, pp Blood, D.C., Radostitis, O.M., Veterinary Medicine, 7th Ed. Bailliere Tindal, London, UK, pp Burchfield, S.R., Wood, S.C., Elich, M.S., Pituitary adrenocortical response to chronic intermittent stress. Physiol. Behav. 24, Dandliker, W.B., Feigen, G.A., Quantification of the antigenantibody reaction by polarization immunochemistry. Immunochemistry 7, Dandliker, W.B., Saussure, D.V., Review article: fluorescent polarization immunoassay. Theory and experimental method. Immunochemistry 10, Dargartz, D.A., Dewqell, G.A., Mortimer, R.G., Calving and calving management of beef cows and heifers on cow-calf operations in the United States. Theriogenology 61, Dufty, J.H., Determination of the onset of parturition in Hereford cattle. Aust. Vet. J. 47, Fischer, H., Bodhipaksh, P., Reproduction in Swamp Buffaloes. In: Tulloh, N.M., Holmes, J.H.G. (Eds.), Buffalo Production, 1st Ed. Elsevier Science Publisher, Amesterdam, Netherland. Hafez, E.S.E., Reproduction in Farm Animals, 6th Ed. Lea & Febiger, Philadelphia, PA. Jainudeen, M.R., Hafez, E.S.E., Reproductive Failure in Females. In: Hafez, E.S.E. (Ed.), Reproduction in farm animals, 6th edition. Lea & Febiger, Philadelphia, PA. Jackson, P.G., Normal Birth of the Cow. Hand Book of Veterinary Obstetrics. W.B. Saunders, London, UK, pp Kharche, K.G., Swingh, H.N., Thakur, M.S., Studies on symptoms and process of parturition in gir cows. Cheiron 11, Kindahl, H., Kornmatitsuik, B., Konigsson, K., Gustafsson, H., Endocrine changes in late bovine pregnancy with special emphasis on fetal well being. Anim. Endocrinol. 23, McDonald, L.E., Veterinary Endocrinology and Reproduction, 1st Ed. Lea and Febiger, Philadelphia, PA, Mukasa, M., Mattoni, M., Parturient behaviour and placental characteristics of Bos indicus cows. Rev. Eleve. Med. Vet. Pays. Trop. 43, Nix, J.M., Sapitzer, J.C., Grimes, L.W., Burns, G.L., Plyler, B.B., A retrospective analysis of factors contributing to calf mortality and dystocia in beef cattle. Theriogenology 49, O Mary, C., Hillers, J., Factors affecting time intervals in parturitions in beef cattle. J. Anim. Sci. 42, Patterson, D.J., Bellows, R.A., Burfening, P.J., Carr, J.P., Occurrence of neoatal and postnatal mortality in range beef cattle. Part I: calf loss incidence from birth to weaning bachward and brench presentations and effect of calf loss on subsequent pregnancy rate of dams. Theriogenology 28, Radostits, O.M., Lesli, K.E., Fetrow, J., Herd Health. 2dn Ed., UK, Rivest, S., How circulating cytokines trigger the neural circuits that control the hypothalamic-pituitary adrenal axis. Psychoneuroendocrinology 26, SAS, Statistical analysis system. User s Guide: Statistics. Version 6, 2nd Ed. SAS Inst. Inc., Cary, NC, Sathya, A., Prabhakar, S., Ghuman, S.P.S., Effect of dexamethasone administration on cortisol concentration and biochemical profile in buffaloes suffering from dystocia. Anim. Reprod. 2, Senger, P.L., Placentation, the endocrinology of gestation and parturition in: Pathways to pregnancy and Parturition, 2nd ed. Current Conceptions, Inc., 320. Stephens, D.B., Stress and its measurements in domestic animals. Adv. Vet. Comp. Msd. 24, Tulloch, D.G., Parent-Offspring Behaviour in Feral Water Buffaloes in Australia, 2nd Ed. World buffalo congress, New Delhi, India. Tulloch, D.G., Behaviour of non-domesticated swamp buffaloes in Australia. In: Tulloh, N.M., Holmes, J.H.G. (Eds.), Buffalo Production. Elsiever Science, Amsterdam, pp Wehrend, A., Hofmann, E., Bostedt, H., The duration of expulsion and the separation of the afterbirth in breeding cows: a contribution to the improvement of parturition monitoring. Deutsch. Tierarztl. Wochenschr. 112, Wehrend, A., Hofmann, E., Failing, K., Bostedt, H., Behaviour during the first stage of labour in cattle: influence of parity and dystocia. Appl. Anim. Behav. Sci. 100, Wittum, T.E., Salman, M.D., Odde, K.J., Mortimer, R.G., King, M.E., Causes and costs of Calf mortality in Colorado beef herds participating in the national Animal Health Monitoring System. J. Anim. Vet. Med. Assoc. 203,

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