Does floor heating around parturition affect the vitality of piglets born to loose housed sows?

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1 Applied Animal Behaviour Science 99 (2006) Does floor heating around parturition affect the vitality of piglets born to loose housed sows? Jens Malmkvist a, *, Lene Juul Pedersen a, Birthe Marie Damgaard a, Karen Thodberg a, Erik Jørgensen b, Rodrigo Labouriau b a Department of Animal Health, Welfare and Nutrition, Danish Institute of Agricultural Sciences, P.O. Box 50, 8830 Tjele, Denmark b Department of Genetics and Biotechnology, Danish Institute of Agricultural Sciences, P.O. Box 50, 8830 Tjele, Denmark Accepted 11 October 2005 Available online 9 November 2005 Abstract The most critical period for the survival of piglets is during the first 2 days of life. Causes of early piglet mortality include reduced vitality due to hypoxia during parturition, hypothermia and lack of adequate colostrum intake. Besides, low vitality piglets may run a larger risk of being crushed by the sow. In the light of the thermoregulatory challenges facing newborn piglets and the possible sowpiglet interactions under loose housing, we investigated whether floor heating around parturition affected early piglet vitality and behaviour related to survival. Twenty-three Landrace Yorkshire sows of 2nd parity were housed individually in 7.5 m 2 pens in a climate controlled facility. HEAT sows (n = 12) were exposed to pen floor heating (33.5 8C) from 12 h after onset of nest building and until 48 h after birth of 1st piglet, whereas CONT sows (n = 11) received no floor heating (21.2 8C). The concentration of lactate in umbilical cord blood at birth an indicator of hypoxia increased with the birth duration (P < 0.001) and with declining piglet weight (P < 0.001), with no significant effect of floor heating. After the initial drop in body temperature at birth, floor heating resulted in an earlier recovery of piglet temperatures (P < 0.001), i.e. the piglet s period for experiencing hypothermia after birth was reduced. HEAT piglets also suckled sooner than CONT piglets after the 1st hour post partum (with ratios between HEAT/CONT hazard functions being for latency to suckle in the period 1 3 h after birth). Moreover, fewer live-born piglets died during the first 3 days (P = 0.047), as well as during the first week in the floor heated litters * Corresponding author. Tel.: ; fax: address: jens.malmkvist@agrsci.dk (J. Malmkvist) /$ see front matter # 2005 Elsevier B.V. All rights reserved. doi: /j.applanim

2 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) (mean (S.E.) HEAT 8.7 (2.8)% versus CONT 15.5 (5.2)%, P = 0.014). We did not find any effect of floor heating on duration of parturition, inter-birth intervals, litter size, early piglet weight gains, blood glucose and lactate concentrations at birth, heart rate at birth, piglet activity from birth to first suckling or amount of parvovirus antibodies transferred from sow to piglets. In conclusion, floor heating around parturition had no evident effect on the innate piglet vitality, but it had favourable effects on the early recovery of piglet body temperature, latency to first suckle and survival of piglets in the loose house system. # 2005 Elsevier B.V. All rights reserved. Keywords: Sus scrofa; Piglet viability; Thermoregulation; Mortality 1. Introduction Piglets experience a sudden drop in their ambient temperature at birth (Berthon et al., 1994), resulting in a reduced body temperature in the early period (h) after birth. This hypothermia in neonatal pigs is promoted by a wet heat conduction surface, their poor insulation combined with a poor ability to thermoregulate, due to low amounts of mobile lipids/glycogen reserves and no brown adipose tissue for metabolic heat production (Svendsen et al., 1986; Herpin et al., 2002). English and Morrison (1984) suggested that heat loss in piglets may be reduced by peripheral vasoconstriction, but this could not be verified in measures of blood flow directed to the skin during cold exposure on the first day of life (Herpin et al., 2002). Piloerection is presumably ineffective for heat conservation due to the poor hair coverage in the domestic pig. Thus, piglets are energetically vulnerable and must overcome hypothermia shortly after birth. When exposed to temperatures below thermoneutrality (around C), neonatal pigs partly rely on muscular thermogenesis in terms of shivering, the efficiency of which gradually improves during the first 5 days after birth (Berthon et al., 1994). Behavioural thermoregulation also develops after birth and includes actively seeking warm places and huddling with littermates. Initiation of suckling is essential for the early provision of both heat and energy to the piglet, in particular for piglets born with a low vitality which in addition may increase their vulnerability. Under natural conditions, the heat requirement of piglets is partly met by staying in the nest, where the temperature is higher than the surrounding environment in cold climates. The piglets stay in the nest close to the sow during the majority of the time on the first days after farrowing (Algers and Jensen, 1990; Stangel and Jensen, 1991). Under production conditions, the thermal environment can be challenging for the neonatal piglet, due to the lack of nest and insulating material in many systems. To compensate for this, a heated piglet area is often provided in the pen. However, the use of this piglet area or creep is reported to be low during the first couple of days after birth (Møller et al., 2001; Pedersen et al., 2005), and the attraction to a radiant heat source (commonly used in piglet creeps) is poor, at least when compared to huddling with other piglets during the first days of life (Hrupka et al., 2000). Herpin et al. (2001) also observed that piglets ignored the warm environment provided under the infrared lamps during the first postnatal hours. Besides, ambient temperatures around C are usually recommended in farrowing houses,

3 90 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) since higher temperatures are suggested to reduce the feed intake and milk production of sows as the period of lactation proceeds (Biensen et al., 1996; Svendsen and Svendsen, 1997; Barnett et al., 2001). The sows may, however, have a higher temperature preference closer to the thermoneutrality zone of newborn piglets around parturition. This hypothesis is supported by studies showing that sows do not avoid high temperatures at farrowing (Pedersen et al., 2005), and may even prefer to rest in areas with high temperatures ( C) during the first days after farrowing when given a choice (Phillips et al., 2000; Pedersen et al., 2005). The most critical period for the survival of piglets is during the first 2 days of life, observed across several types of housing (e.g. Bereskin et al., 1973; English and Smith, 1975; Svendsen et al., 1986; Kongsted and Larsen, 1999; Barnett et al., 2001). The major causes of early piglet mortality are reported to be hypoxia during parturition, lack of adequate colostrum intake, and crushing by the sow (English and Smith, 1975; Svendsen et al., 1986; Fraser, 1990; Herpin et al., 1996; Edwards, 2002). However, these causes of death often seem to be triggered by an inadequate thermal environment postnatally leaving the piglets at risk of hypothermia. Hypothermic piglets are less vital and their chances of getting access to the udder and avoiding the movement of the sows are thus reduced (Herpin et al., 2002). This may be even more difficult for piglets in loose housing systems due to the possibility of the sow moving around in the pen. In the light of these thermoregulatory challenges facing newborn piglets, we investigated whether floor heating around parturition of loose housed sows affected early piglet vitality and behaviour related to survival. 2. Materials and methods 2.1. Animals, housing and management We housed pregnant Landrace Yorkshire sows (n = 28) of second parity individually in 7.5 m 2 pens in a climate controlled facility, from 1 week before expected parturition (i.e. day of gestation) until 1 week after farrowing. A water-based heating system was built into the concrete pen floor, and a heat mat (Model ESS-004, 230V, from Rexlan Europe, DK Soroe, Denmark) with piglet access only was included in all pens (Fig. 1). All sows had been loose housed during their first farrowing, and were similarly housed prior to the experiment. The sows were fed twice daily with a standard amount and type of dry concentrate sow feed, and had access to water ad libitum. One kilogram of long barley straw was provided daily in a straw rack, if less than 0.5 kg was left. The house had an average (S.D.) air temperature of 21.2 (0.8) 8C with a relative humidity of 47.6 (8.1)%, and was exposed to some natural daylight ( N, E) from windows, combined with 24 h artificial lighting during the experimental period between February 16 and May 12, Experimental protocol and inclusion criteria Half of the 28 sows were randomly chosen to be exposed to floor heating 12 h after the onset of nest building until 48 h after the birth of the first piglet (group: HEAT ), whereas

4 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Fig. 1. The farrowing pen for one sow with her litter. The height of the side walls was 1.2 m, with three solid wooden walls and a barred front wall with a straw rack mounted on the entrance door. The piglet area with permanent heat was separated with bars from the rest of the pen, with a free entrance height of 17 cm. Temperature in the floor was recorded by two built-in sensors. the rest of the sows entered the control group ( CONT ) with no floor heating. The temperature measured by built-in floor sensors (Fig. 1) averaged (S.D.) 21.1 (1.4) 8C for the CONT treatment and 33.5 (1.6) 8C for the HEAT treatment during the 48 h after the birth of the first piglet. We evaluated signs of nest building twice a day at 8 and 20 h using digital video surveillance recordings. The onset of nest building was defined as the first occurrence of at least five front leg pawings per hour or repeated carrying of straw, without being interrupted by resting periods longer than 2 h (modified from Thodberg et al., 2002 and Pedersen et al., 2003). As a consequence of the individual variation in the duration from start of nest building until the beginning of the farrowing, the HEAT sows were exposed to floor heating for a variable amount of time, on average (S.E.) 17 h 38 min (4 h 20 min), prior to the birth of the first piglet. The criteria for sows to enter the experiment were a minimum delivery of eight liveborn piglets, and being in a good health condition, i.e. sows receiving medical treatment a week before and during parturition were excluded. Hence, the results are based on litters from sows needing neither human nor pharmaceutical aid during farrowing. In total, five out the original 28 sows were excluded due to medical treatment/farrowing assistance (2 CONT, 1 HEAT sows), too few live-born piglets (1 CONT sow) and because floor heating by mistake was activated too late prior to farrowing (1 HEAT sow), reducing the number of sows to 23 (CONT: n =11,HEAT:n = 12). The body weight of the 23 sows did not differ between treatments (CONT: 250 (5.1) kg versus HEAT: 247 (4.1) kg, t 21 =0.39, P =0.70).

5 92 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Other handling We moved piglets from litters with more than 14 live piglets (i.e. the number corresponding to the number of teats) 25 h after birth of the first piglet. The surplus piglets were chosen randomly and removed to foster sows outside the experiment and room. Day 4 after birth, all piglets were injected with vitamins, ear marked, tail docked and the males were castrated. Other management practices, such as placement of piglets at the udder or in the heated piglet area, rescue of piglets when trapped beneath the sow, were avoided. The experiment presented here was part of a larger project, and therefore all sows were catheterised on gestation day by the method described by Damm et al. (2000). From the day after catheterisation until week 1 after farrowing, daily blood samples were taken prior to morning feeding around 08:00 h. In addition, from 12 h after the onset of nest building until 24 h after the birth of the first piglet, blood was sampled hourly from the sow s catheter. This sampling could be carried out with minimal disturbance, and the data on sow physiology will be reported elsewhere (Damgaard et al., in preparation). The entire experiment was approved for and controlled by the Danish Animal Experiments Inspectorate (Journal no. 1999/561-20) Sampling and behavioural observations The time course of the sampling for each individual piglet is summarized in Table 1.We took the newborn piglet when it reached the floor after birth. The sampling events were initiated in the order indicated in Table 1. However, to shorten the handling duration the sampling occurred simultaneously whenever possible, e.g. by measuring heart rate while taking umbilical cord blood. The mean (S.E.) handling duration from birth to first suckling was 6 min 40 s (12 s), and did not differ between treatment (F 1,20 = 0.6, P = 0.44). After sampling each piglet was Table 1 Sampling events for each individual piglet from birth to day 7 Time of sampling Sampling event Comment At birth, T = 0 Time of birth Piglet free of rima vulva State of umbilical cord Ruptured or whole Blood from umbilical cord For lactate and glucose determination Heart rate Counted for 15 s Blood drop taken from ear For glucose determination Rectal temperature Marking on back For individual piglet identification Body weight T + 30 min, +1 h, +2, +4, +8, +24 h Rectal temperature Blood drop taken from ear For glucose determination T + 8, +24 h Body weight T = 0 to first suckling Behavioural observations From video recordings (see Table 2) T = 0 to day 7 Collection of dead Day 7 Blood sampling For determination of PPV antibodies

6 returned to the same place where it had been picked up. It was not always possible especially for older piglets to ensure that they were in the same posture after as before handling. For the individual piglets, we defined birth duration for each piglet as the time passed since the first piglet was born, inter-birth interval for each piglet as time since previous piglet was born, and being live-born as having detectable heart beat at birth. For the litter as a whole, we use the term duration of parturition for the duration from first to last born piglet, average inter-birth interval for the average of the inter-birth intervals, and S.D. inter-birth interval for the standard deviation in the inter-birth intervals of the piglets within a litter. Total number born is all piglets delivered regardless of being alive (having heart beat) or not, and Mortality is the proportion between the number of live-born piglets dead at a given time and the number of live-born at birth for the litter Blood from the umbilical cord for determination of lactate and glucose concentrations at birth Immediately after birth, ml blood were drawn from the umbilical cord using a heparinized blood gas syringe (type QS50, Radiometer, Copenhagen, Denmark) with a 19 gauge 35 mm needle, without rupturing the cord. Afterwards non-ruptured umbilical cords were carefully detached, by pulling it slowly keeping the hands close to the sow s vulva. Care was taken to minimize sample contamination with air and to expel air bubbles if any, before the syringe opening was sealed with a screw cap after collection. We completed the sampling in average (S.E.) 2.2 (0.12) min after birth. Samples sealed later than 8 min after birth were not used in the data analysis. The blood-filled syringe was placed on ice until analysis, occurring on average (S.E.) 2.4 (0.07) h after collection. The concentration of lactate and glucose was analysed using a blood metabolite analysing system (ABL System 625/615/605, Radiometer, Copenhagen, Denmark) Heart rate J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Heart rate was monitored using an electronic stethoscope (M30 from Meditron Stethoscopes AS, N-1392 Vettre, Norway) and also by hand. This was easy with regard to most of the piglets; it was, however, difficult to count accurately the heart beats faster than approximately 60 beats per 15 s, observed in 14.2% of the born piglets Determination of glucose concentration (T = 0, 1/2, 1, 2, 4, 8, 24 h after birth) Using lancets for skin puncture (HemoCue Safety lancets), one drop of blood was collected from a vein in the piglet ear into a microcuvette (5 ml) for measurement. Within 40 s the glucose concentration was determined photometrically based on a modified glucose dehydrogenase method, using the portable HemoCue B-Glucose Analyzer (HemoCue Denmark, DK-2940 Vedbaek). In a pilot study, we compared the HemoCue method and the blood analyser system of our laboratory (ABL System 625/615/605, Radiometer) using venous blood collected in 3-day-old piglets. The two methods were linearly and highly correlated (R 2 = 0.98, P = 0.004, 5 piglets) in the test range of (mean (S.E.) 6.9 (0.31)) mmol glucose/l (ABL).

7 94 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Rectal temperature (T = 0, 1/2, 1, 2, 4, 8, 24 h after birth) The rectal temperature was measured using a lubricated digital thermometer (Omron flex temp, precision 0.1 8C) introduced approximately 1 cm into the rectum of the piglet Behaviour of piglets from birth to first suckling Each individual piglet was continuously observed from video recordings in the period from birth and until first suckling, defined as the piglet having the whole nipple in the mouth for at least 5 s, apparently with milk ingestion. Not all piglets did suckle, and observations stopped when the piglet was removed as dead. The behaviour of piglets was scored from digital video recordings by observers blind with regard to the experimental treatment, using the ethogram in Table Blood sampling for determination of porcine parvovirus (PPV) antibodies day 7 All experimental sows had been vaccinated with an inactivated PPV vaccine (PPVvaccine Vet., Danish Veterinary Institute, Lindholm, Denmark) approximately 6 and 3 weeks prior to mating. The level of serum antibody titre was measured in both sow and piglets day 7 after birth. Sera from 10 ml venous blood were stored in plastic tubes at 20 8C until assayed for PPV antibodies (PPV-ab) using a blocking enzyme-linked immunosorbent assay (ELISA) as described in Madsen et al. (1997). The serum PPV-ab in piglets are dependent on the levels of PPV-ab in the sow, because of the transfer from sow to piglet via the early colostrum (Damm et al., 2002) Statistics Treatment effects on the duration of parturition, average inter-birth interval, S.D. interbirth interval, inter-birth interval, lactate and glucose concentrations, heart rate at birth, piglet weight gains, behaviour, and ratio of piglet to sow PPV-ab were analysed using a normal linear mixed model with the effect of sow within treatment as random effect when observations of individual piglets were analysed. The P values reported from the mixed models are based on the Satterthwaite approximation for the denominator degrees of freedom. The calculations were made using the Mixed procedure in the SAS software (8.02, SAS Institute, Cary, NC; Littell et al., 1996). The total number born and the number Table 2 Piglet behaviour from birth until first suckling observed from digital video recordings Behaviour Definition Active in pen Moving around, not being passive and not in udder contact Passive in pen Lying inactive for a minimum of 5 s and not in udder contact Udder contact Body in contact with the udder of the sow, between front to hind leg, without suckling Trapped Trapped by the sow, i.e. by the limbs or beneath the body of the sow Suckling Teat in the mouth for at least 5 s Away from pen Being handled due to sampling, or removed as dead

8 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) of live-born piglets per litter was analysed using a Poisson distribution, and the proportion of piglets dying (litter mortality) was analysed with binomial logistic regression using generalized estimating equations (GEE) based inference to take into account the dependency induced by the litter structure (Liang and Zeger, 1986). The calculations were made using the procedure Genmod in SAS. The demand for dispersion and variance homogeneity was tested, and the validity of the final model judged by the appearance of the residuals. Table 3 summarizes the covariates and the treatment covariate interactions included in the models. The models were reduced by stepwise removal of insignificant terms (P > 0.10), starting with the interactions. Significant effects of the covariates or interactions between the treatment (CONT, HEAT) and covariates are presented in the text. Development in rectal temperature and glucose concentration 0 24 h was analysed using an extension of the linear mixed model presented above. To obtain a flexible curve, a natural cubic spline (Hastie, 1993) were used to fit the development over time for each treatment, and the repeated measurements on each piglet were taken into account using an unstructured covariance matrix in addition to the random effect of sow. The residual variance was estimated separately for each planned observation time, and in addition, the glucose measurements were transformed using the square root. The spline basis was formulated on the basis of square root of observation time and had breakpoints at the planned observation times with 0 and 25 h as boundary points. The effect of treatment on development was tested by comparing the model with treatment specific development with a model with identical development for the two treatments using a likelihood-ratio test. These calculations were made using R (R Development Core Team, 2005) and the function lme in the nlme library (Pinheiro et al., 2005). Table 3 Covariates included in modelling treatment effects Covariate Range Included in model for the response variables Duration of parturition min Number of live-born a, total number born a, mortality a Number of stillborn 0 4 Number of live-born a, mortality a, duration of parturition a, inter-birth interval a S.D. in inter-birth interval 8 40 min Number of live-born a, total number born a, mortality a Sow weight at entry kg Number of live-born, total number born, mortality, duration of parturition, inter-birth interval Number of live-born Duration of parturition a, inter-birth interval a Birth duration min Lactate a, glucose at birth a, heart rate a, weight gains a, behaviour a Inter-birth interval min Lactate a, glucose at birth a, heart rate a, weight gains a, behaviour a Piglet weight at birth kg Lactate a, glucose at birth a, heart rate a, weight gains a, behaviour a Status of umbilical cord Ruptured or whole Lactate a, glucose at birth a, heart rate a Blood sampling duration 0 8 min Lactate, glucose at birth Storage time until analysis min Lactate, glucose at birth Lactate concentration mmol/l Heat rate a, behaviour a, PPV-ab ratio a Glucose concentration at birth mmol/l Heart rate a a Interaction between treatment and the covariate included in the start model.

9 96 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Latency to the first suckle was analysed using methods of survival analysis considering censored data (Kalbfleisch and Prentice, 2002). Piglets for which no suckling was observed were taken as right censored observations. The model assumed a piecewise constant hazard function (i.e. instantaneous velocity to suckle) at each 5-min interval. We define the hazard ratio as the ratio between the hazard functions for HEAT and CONT piglets, and these ratios were estimated at each interval of 30 min from birth until 4 h after birth. The inference was adjusted for birth weight, birth duration, and lactate concentration. The calculations were made using a function in R (R Development Core Team, 2005) specially designed for the present analysis. A probability level (P) of 0.05 was chosen as the limit for statistical significance in all tests. P values of are reported as tendencies. Means are given with S.E. and model estimates are given with 95% confidence intervals. 3. Results 3.1. Duration of parturition, inter-birth intervals, litter size, piglet weight gains, and mortality The results of these variables are summarised in Table 4. Out of the 358 piglets delivered in total, 77 piglets died during the experimental period (days 0 7); and 32.5% of these were stillborn. We found no difference in the total number and number of live-born piglets between treatments. The proportion of live-born piglets dying (mortality) day 0 7 was higher in the CONT than in the HEAT group (P = 0.014; Table 4). Besides, the mortality increased with increasing duration of parturition (P < 0.001) and decreased with increased S.D. in inter-birth interval (P = 0.001). The adjusted mortality for days 0 7 (for a hypothetical litter with average duration of parturition and average S.D. in inter-birth interval) is estimated to 12.3% ( %) for CONT-litters and 5.1% ( %) for HEAT-litters. When the period from days 0 to 3 was considered separately, the same significant effects of treatment (P = 0.047), duration of parturition (P < 0.001), and S.D. in Table 4 Results as mean (S.E.) for litters without (CONT) or with (HEAT) floor heating around parturition CONT HEAT Test statistics P-value Duration of parturiton (min) 251 (17) 272 (42) F 1,21 = Avg. inter-birth interval (min) 20.1 (2.28) 19.5 (2.23) F 1,17.5 = Total no. piglets born per litter 16.4 (0.83) 15.4 (0.93) x 2 21 = No. live-born piglets per litter 15.7 (0.91) 14.8 (0.83) x 2 20 = Piglet weight gain (g) 0 8 h 39 (12.0) 19 (10.0) F 1,12.6 = h 59 (11.0) 50 (14.0) F 1,18.9 = Mortality (%) Days (4.55) 7.2 (2.79) x 2 17 = a Days (5.23) 8.7 (2.76) x 2 17 = a a Significant difference between treatments.

10 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Table 5 Concentration of lactate and glucose in umbilical cord blood, and piglet heart rate at birth, as mean (S.E.) and [minimum maximum] values CONT HEAT Test statistics P-value Lactate (mmol/l) 4.9 (0.26) [ ] 4.6 (0.23) [ ] F 1,20.2 = Glucose (mmol/l) 3.0 (0.08) [ ] 2.8 (0.10) [ ] F 1,19 = Heart rate (bpm) 196 (3.6) [44 324] 196 (3.3) [ ] F 1,19 = inter-birth intervals (P < 0.001) were found for mortality. Naturally, the number of dead piglets days 0 3 is included in and correlated with the mortality in the entire experimental period, days 0 7 (Pearson r = 0.892, P < 0.001). There was no treatment effects on the percentage of stillborn piglets (F 1,21 = 1.8, P = 0.18) ranging from % per litter. We did, however, not systematically differentiate between pre- and intra-partum stillbirths. At least 20% of the collected stillborn piglets had been dead for a while and not during parturition, since they were noted to be decomposed/decayed/old, but this registration was not done systematically for all litters. Since treatment effects, if any, are to be expected on the intrapartum stillbirths, our data are not particularly useful in that respect. The birth weight positively affected weight gain 0 8 h (F 1,172 = 4.1, P = 0.043) and 0 24 h (F 1,235 = 25.2, P < 0.001). Besides, piglet weight gain decreased with increasing interbirth intervals (F 1,220 = 6.2, P = 0.014) during the first 24 h. We found no effects of floor heating on the weight gain of piglets (Table 4) Concentration of lactate and glucose in the umbilical cord and heart rate at birth The major results on blood parameters and heart rate are presented in Table 5. The lactate concentration did not differ between treatments (P = 0.57), but increased with birth duration (F 1,233 = 36.0, P < 0.001) and decreased with increasing piglet body weight (F 1,223 = 21.0, P < 0.001). We found no effect of floor heating on the glucose concentration at birth (P = 0.41), whereas the concentration increased with birth duration (F 1,242 = 39.0, P < 0.001) and with inter-birth interval (F 1,229 = 5.7, P = 0.018). We found no effect of treatment on the heart rate of newborn piglets (P = 0.84). Heart rate at birth was lowered with increases in lactate concentration (F 1,238 = 6.8, P = 0.001), whereas a long birth duration only tended to increase the heart rate (F 1,225 = 3.2, P = 0.074) Rectal temperatures and blood glucose in the period 0 24 h The development in rectal temperature was significant different between CONT and HEAT piglets (x 7 = 31.6, P < 0.001; Fig. 2). HEAT piglets recovered sooner from the initial drop in body temperature after birth. The temporal development in glucose concentration in the blood of piglets in the first 24 h also showed differences between treatments (x 7 = 15.9, P = 0.026) starting out at the same level and reaching a slightly higher level in the control treatment (Fig. 3). The proportion of observations with very high glucose levels (greater than 12 mmol/l) was higher in CONT piglets (25 versus 7; x 2 1 = 9.2, P = 0.002). Glucose values above 14 mmol/l were observed 10 times (out of 1083

11 98 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Fig. 2. Rectal temperature the first 24 h after birth. CONT: black, and HEAT: red colour. Only a random sample of 500 data points is shown to avoid cluttering of the figure. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.) observations) in CONT piglets, but only once (out of 1089 observations) in HEAT piglets Piglet behaviour from birth until first suckling The majority of live-born piglets (98.8%) touched the udder, and no difference between the treatments in the latency to udder contact was found (CONT 28.3 (3.03) versus HEAT Fig. 3. Glucose concentration in the first 24 h after birth. CONT: black, and HEAT: red colour. Only a random sample of 500 data points is shown to avoid cluttering of the figure. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)

12 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Fig. 4. Cumulative probability of suckling in the first 8 h after birth. CONT: black, and HEAT: red colour, with 95% confidence intervals (dotted lines). The vertical line indicates the end of the period with no difference between CONT and HEAT piglets in the latency to suckle (cf. Table 6). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.) 29.3 (3.18) min; F 1,18.6 = 0.85, P = 0.37). Fig. 4 illustrates the cumulative probability of first suckling over time. We found no difference in hazard ratio for suckling during the first hour after birth, while HEAT piglets initiated their first suckling sooner than did CONT piglets after the first hour post partum. Hazard ratios greater than 1 (Table 6) indicate that HEAT sooner than CONT piglets initiated suckling in several periods after birth. Results of the behavioural observations on piglets are summarised in Table 7. We found no difference Table 6 Hazard ratios (the ratio of HEAT/CONT hazard fuctions) for latency to suckle (95% confidence interval) Time after birth (h) Hazard ratio HEAT/CONT P-value ( ) ( ) ( ) <0.001 a ( ) <0.001 a ( ) ( ) a ( ) ( ) 0.39 The P-values are for testing the hypothesis of hazard ratio (HR) = 1, i.e. being equal for HEAT and CONT piglets. Significant HR > 1 indicates that HEAT piglets suckle sooner than CONT piglets. a Significant difference between treatments.

13 100 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Table 7 Piglet behaviour observed from birth until first suckling Behaviour CONT HEAT Test statistics P-value Active in pen (% time) 51.1 (1.98) 52.9 (1.79) F 1,18.7 = Passive in pen (% time) 11.7 (1.65) 9.5 (1.26) F 1,19.2 = Contact with udder (% time) 36.8 (2.04) 36.3 (1.96) F 1,17.9 = Proportion of piglets trapped (%) x 2 1 = Proportion of live-born piglets suckling (%) x 2 1 = in the average observation time between piglets from the two groups (CONT 58.2 (6.05) versus HEAT 50.8 (6.66) min; F 1,19.9 = 0.2, P = 0.70). We observed only few incidents of piglets being trapped per litter (CONT 0.1 (0.03) versus HEAT 0.2 (0.04), x = 0.6, P = 0.44) in the period from birth to first suckling. Therefore, observations during a longer period and in particular on more litters are probably needed to detect differences in trapping and crushing of piglets Porcine parvovirus antibodies (PPV-ab) in piglets The ratio between piglet and sow serum PPV-ab declined with increasing concentration of lactate in the umbilical cord at birth (F 1,183 = 16.5, P < 0.001). Besides, the ratio of PPV-ab declined with increasing birth durations in the HEAT, but not significantly in the CONT piglets (interaction between treatment and birth duration; F 1,189 = 6.4; P = 0.012). 4. Discussion Our results indicate that floor heating (around C) during the first 48 h after parturition is favourable for the neonate pig, since it resulted in earlier recovery of piglet body temperature, reduced the latency to first suckle, and lowered mortality. We expected that the high floor temperature would stress the sows in late-pregnancy, with potential effects on the farrowing and the vitality of piglets at birth. However, this hypothesis was not supported by our results on farrowing variables, the lactate concentration, and the other variables measured in piglets at birth. Thus, even though the HEAT sows may have experienced some level of mild stress due to the increase in floor temperature during the parturition (Damgaard et al. (in preparation) found a transiently more variable and higher mean plasma cortisol concentration in HEAT than in CONT sows during the period from 8 h before until 24 h after the birth of first piglet), this has not been to an extent where piglets suffered from e.g. hypoxia due to prolonged birth durations. Piglets born on the heated floor suckled sooner than control piglets. Thus, floor heating had a favourable effect on the initiation of suckling in those (approximately one-third of the) piglets, which had not yet suckled within the first hour post partum. The earlier initiation of suckling is probably a consequence of the earlier recovery in the rectal temperature observed in HEAT piglets. Normally, the drop in body temperature at birth is recovered when the piglets successfully obtain colostrum and their ability to thermoregulate is developed. Piglets which have not ingested colostrum or which are very

14 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) small at birth are therefore particularly prone to hypothermia (Herpin et al., 1996). Floor heating may have kept these piglets warmer until they could achieve their first suckling event. In contrast, piglets born on a cold floor may be chilled, late to achieve their first suckling event, and receive less colostrum; factors known to impair their ability to thermoregulate (Le Dividich and Noblet, 1981); as a consequence some of them will be fatally weakened. This course of events is supported by the finding that a higher proportion of piglets died in the CONT than in the HEAT group. One may have expected to find a lower colostrum intake in the CONT piglets. This was found by Le Dividich and Noblet (1981) using warm and cold piglets, Parker et al. (1980) in cold-stressed piglets, and Damm et al. (2002) also reported that piglet PPV-ab decreased when time to first suckling event increased. However, we did not find such a difference in our study, using piglet PPV-ab as an indicator of early colostrum intake. The reason for this may be that more of the piglets at risk of low colostrum intake die in the CONT group, whereas these piglets survive in the HEAT group, until the PPV-ab determination at day 7. This would blur the potential treatment effects on the measures of early colostrum intake. As may be expected, we found that the glucose concentration at birth increased with long birth durations and long inter-birth intervals of piglets, indicating a mobilisation of glucose during prolonged or troubled course of parturition. Likewise, Herpin et al. (1996) reported higher glucose concentration in low compared to high vitality piglets (based on evaluation of heart rate, breathing rate, skin colour and intensity of standing behaviour 1 min after birth). In our study, while not different between treatments at birth, control piglets developed a slightly higher mean glucose concentration in the blood during the first 24 h after birth. This may suggest that CONT piglets are less vital in the period after birth. However, both low and high glucose concentrations may be a result of adverse effects during the period after birth, since hypoglycaemia could be a result of not receiving an adequate supply of energy from colostrum and hyperglycaemia could be a result of the mobilisation of glycogen stores in stressed and dying individuals (Svendsen et al., 1986; Herpin et al., 1996). This should be taken into account, when one interprets the mean glucose concentration of the two treatment groups; in our study, values exceeding the normal range of glucose were mainly observed in the control piglets. The drop in body temperature was greatest 30 min after birth, and normalised for most (surviving) piglets within the first 8 24 h after birth. In farrowing pens, heat lamps are often provided in creeps within the pen, and these facilities improve the thermal environment for those piglets that reach them. However, it is difficult to ensure that all piglets move into this heated area during the first postnatal hours, during which piglets should sample colostrum (Algers, 1993), which is of importance also for developing their thermoregulatory ability (Herpin et al., 1996). Furthermore, piglets in need of energy may spend more time in risky areas close to the sow (Weary et al., 1996). Therefore, floor heating at birth may in particular be advantageous, since it requires no additional effort of the piglet to access it and may allow piglets to rest close to the sow with less risk of being chilled or injured, i.e. enable them to obtain colostrum with a reduced chance of being crushed. Our results underline the impact of thermal conditions during the early hours after birth, even with effects on the long-term survival of the individual. We have not analysed the postural changes of the sows in the present study, but sows in pens with partly heated floor (35 8C) had significant fewer postural changes compared to

15 102 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) sows in unheated pens, while their general level of activity was unaffected by floor heating, on the first day after farrowing (Pedersen et al., 2005). Considering piglet crushing, the proportion of piglets being trapped underneath the sow before their first suckling appears high (10 13%) in our study, also since sows may have relatively few posture changes during the early period, when farrowing is still in progress and colostrum is constantly available (Pedersen et al., 2003). However, it should be recognised that our definition also included incidences with little effect on the piglets (Table 2), as indicated by the observations of piglets being trapped more than once and still surviving. In 43 out of the 45 observed trappings, the affected piglet initiated suckling afterwards. Thus, the early trapping of piglets by the sow could not explain the treatment effects on mortality in our study. Several measures of vitality in piglets at birth have previously been used (for further discussion see e.g. Zakeski and Hacker, 1993; Herpin et al., 1996). Lactate is an indicator of hypoxia during parturition, and increased with the birth duration and with declining piglet weight in our experiment. The ability to thermoregulate during an acute cold stress has been found to be inversely related to the umbilical blood lactate concentration (Stanton et al., 1973). We observed that the lactate concentration may vary broadly between piglets within the same litter. A considerable part of the early postnatal mortality is due to hypoxia (Herpin et al., 1996), and there probably exists a continuum between piglets dying of hypoxia during parturition and piglets of low vitality that die postnatally. The piglets were handled several times during the first 24 h for collection of data (Table 1). Even though each handling episode was of a short duration, this handling regime may blur some of the potential treatment effects on piglet behaviour. However, handling was equal and standardised between treatments, and care was taken to return the piglets to the same spot after data collection. Besides, our latency times for first suckling are comparable to what has been found in litters from loose housed primiparous sows without this piglet handling (approximately 50 min; Pedersen et al., 2003). The sows had access to straw, which is likely to diminish the difference in thermal challenge facing the piglets born in the control versus the heated pens. Therefore, the effects of floor heating on the piglets may be even more prominent under housing conditions with only little or no straw provision. We have no indication of the different amounts of straw used by sows in the two groups. However, Pedersen et al. (2005) did not find any difference in use of straw during nest building in sows with and without a partly heated floor. The main reasons for using straw in our study are that sows are highly motivated to perform nest building prior to farrowing (Jensen, 1993) and also that provision of nest materials may also increase their maternal responsiveness towards piglets (measured 1 3 days post partum; Herskin et al., 1998). The presented results are based on second parity sows with a minimum of eight live piglets at delivery, excluding sows needing medication or farrowing assistance (cf. Section 2). Therefore, the ability of floor heating to reduce piglet mortality should be further verified in larger scale studies, without excluding any sows. It would also be advantageous to evaluate the effects on sow and piglets in a range of ambient temperatures. The relatively high litter size of the experimental sows (averaged piglets) is not uncommon and reflects the on-going selection for large litters in modern production. The selection has lead

16 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) to a marked increase in the total number of piglets born in the Landrace and Yorkshire, but also to an increase in piglet mortality (Su et al., 2004). The continued increase in litter size and changes related to it (such as reduced piglet size and longer birth durations leading to increased risk of hypoxia) may in accordance with the current knowledge increase the proportion of piglets at risk of hypothermia and a low colostrum intake. Thus, we expect an increasing demand for a good thermal environment immediately at birth and in the early period thereafter, to ensure the welfare and survival of piglets. 5. Conclusion Floor heating around parturition had no evident effect on the innate piglet vitality, but it had favourable effects on the initiation of suckling (in particular for a group of apparently weaker piglets), thermoregulation, and the survival of piglets. We suggest that the treatment effects on piglet survival are verified in larger scale experiments, and under a range of ambient temperatures. Acknowledgement This study was supported by a grant (J.no. 93s-2465-A ) from The Danish Directorate for Food, Fisheries and Agri Business. References Algers, B., Nursing in pigs: communicating needs and distributing resources. J. Anim. Sci. 71, Algers, B., Jensen, P., Thermal microclimate in winter farrowing nests of free-ranging domestic pigs. Livest. Prod. Sci. 25, Barnett, J.L., Hemsworth, P.H., Cronin, G.M., Jongman, E.C., Hutson, G.D., A review of the welfare issues for sows and piglets in relation to housing. Aust. J. Agric. Res. 52, Berthon, D., Herpin, P., Le Dividich, J., Shivering thermogenesis in the neonatal pig. J. Therm. Biol. 19, Bereskin, B., Shelby, C.E., Cox, D.F., Some factors affecting pig survival. J. Anim. Sci. 36, Biensen, N.J., von Borell, E.H., Ford, S.P., Effects of space allocation and temperature on periparturient maternal behaviors, steroid concentrations, and piglet growth rates. J. Anim. Sci. 74, Damgaard, B.M., Malmkvist, J., Pedersen, L.J., Jørgensen, E., in preparation. Effects of thermal environment on feed intake, immune competence and stress response in loose housed sows (Sus scrofa) before, during and after farrowing. Damm, B.I., Pedersen, L.J., Ladewig, J., Jensen, K.H., A simplified technique for non-surgical catheterization of the vena cava cranialis in pigs and an evaluation of the method. Lab. Anim. 34, Damm, B.I., Friggens, N.C., Nielsen, J., Ingvartsen, K.L., Pedersen, L.J., Factors affecting the transfer of porcine parvovirus antibodies from sow to piglets. J. Vet. Med. A 49, Edwards, S.A., Perinatal mortality in the pig: environmental or physiological solutions? Livest. Prod. Sci. 78, English, P.R., Smith, W.J., Some causes of death in neonatal piglets. Vet. Annu. 15, English, P.R., Morrison, V., Causes and prevention of piglet mortality. Pig News Inform. 5, Fraser, D., Behavioural perspectives on piglet survival. J. Reprod. Fertil., Suppl. 40,

17 104 J. Malmkvist et al. / Applied Animal Behaviour Science 99 (2006) Hastie, T.J., Generalized additive models. In: Chambers, J.M., Hastie, T.J. (Eds.), Statistical Models. S. Chapman & Hall Inc., London (Chapter 7). Herpin, P., Dividich, J., Hulin, J.C., Fillaut, M., De Marco, F., Bertin, R., Effects of the level of asphyxia during delivery on viability at birth and early postnatal vitality of newborn pigs. J. Anim. Sci. 74, Herpin, P., Hulin, J.C., Le Dividich, J., Fillaut, M., Effects of oxygen inhalation at birth on the reduction of early postnatal mortality in pigs. J. Anim. Sci. 79, Herpin, P., Damon, M., Le Dividich, J., Development of thermoregulation and neonatal survival in pigs. Livest. Prod. Sci. 78, Herskin, M.S., Jensen, K.H., Thodberg, K., Influence of environmental stimuli on maternal behaviour related to bonding, reactivity and crushing of piglets in domestic sows. Anim. Sci. 68, Hrupka, B.J., Leibbrandt, V.D., Crenshwa, T.D., Benevenga, N.J., The effect of thermal environment and age on neonatal pig behavior. J. Anim. Sci. 78, Jensen, P., Nest building in domestic sows: the role of external stimuli. Anim. Behav. 45, Kalbfleisch, J.D., Prentice, R.L., The Statistical Analysis of Failure Time Data, second ed. John Wiley & Sons, New York. Kongsted, A.G., Larsen, V.A., Pattegrisedødelighed i frilandshold [Piglet mortality in outdoor sow herds]. Report no. 11, Danish Institute of agricultural Sciences, 56 pp. (in Danish, with English abstract). Le Dividich, J., Noblet, J., Colostrum intake and thermoregulation in the neonatal pig in relation to environmental temperature. Biol. Neonate 40, Liang, K.Y., Zeger, S.L., Longitudinal data analysis using generalized linear models. Biometrika 73, Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., SAS System for Mixed Models. SAS Institute Inc., Cary, NC, 633 pp. Madsen, E.S., Madsen, K.G., Nielsen, J., Jensen, M.H., Lei, J.C., Have, P., Detection of antibodies against porcine parvovirus non-structural protein NS1 may distinguish between vaccinated and infected pigs. Vet. Microbiol. 54, Møller, F., Andersen, L., Jensen, L., Pattegrises valg af åben eller lukket hule [Piglets choice of open or closed piglet creep]. Grøn Viden, Husdyrbrug nr. 20, Danish Institute of Agricultural Sciences, 4 pp. (in Danish). Parker, R.O., Williams, P.E.V., Aherne, F.X., Young, B.A., Serum concentration changes in protein, glucose, urea, thyroxine and triiodothyronine and thermostability of neonatal pigs farrowed at 25-degrees-C and 10- degrees-c. Can. J. Anim. Sci. 60, Pedersen, L.J., Damm, B.I., Marchant-Forde, J.N., Jensen, K.H., Effects of feed-back from the nest on maternal responsiveness and postural changes in primiparous sows during the first 24 h after farrowing onset. Appl. Anim. Behav. Sci. 83, Pedersen, L.J., Malmkvist, J., Jørgensen, E., Time development in sow s choice of resting site around parturition in pens with partly heated floor. In: Accepted to the 39th Congress of the International Society of Applied Ethology, Tokyo, Japan. Phillips, P.A., Fraser, D., Pawluczuk, B., Floor temperature preference of sows at farrowing. Appl. Anim. Behav. Sci. 67, Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., nlme: linear and nonlinear mixed effects models. R package version R Development Core Team, R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN , URL: Stangel, G., Jensen, P., Behavior of semi-naturally kept sows and piglets (except suckling) during 10 days postpartum. Appl. Anim. Behav. Sci. 31, Stanton, H.C., Brown, L.J., Mueller, R.L., Interrelationships between maternal and neonatal factors and thermoregulation in fasted neonatal swine (Sus domesticus). Comp. Biochem. Physiol. 44A, Su, G., Lund, M.S., Sørensen, D., Variance components for litter size and survival in Danish Landrace and Yorkshire pigs. In: Proceedings of the 55th Congress of the European Association of Animal Production. Bled, Slovenia, September 5th 9th G pp. Svendsen, J., Svendsen, L.S., Intensive (commercial) systems for breeding sows and piglets to weaning. Livest. Prod. Sci. 49,

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