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Applied Animal Behaviour Science 158 (2014) 16–22

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Applied Animal Behaviour Science


journal homepage: www.elsevier.com/locate/applanim

The effect of ketoprofen on post-partum behaviour in sows


Elina Viitasaari a,c,∗ , Marja Raekallio b,c , Mari Heinonen d , Anna Valros a,c ,
Olli Peltoniemi d , Laura Hänninen a,c
a
Department of Production Animal Medicine, Koetilantie 7, P.O. Box 57, 00014 University of Helsinki, Finland
b
Department of Equine and Small Animal Medicine, Koetilantie 7, P.O. Box 57, 00014 University of Helsinki, Finland
c
Research Centre for Animal Welfare, Koetilantie 7, P.O. Box 57, 00014 University of Helsinki, Finland
d
Department of Production Animal Medicine, Paroninkuja 20, 04920 Saarentaus, Finland

a r t i c l e i n f o a b s t r a c t

Article history: A randomized, double-blinded, placebo controlled trial was conducted in order to estimate
Accepted 13 June 2014 pain-related behavioural changes of sows in early lactation. Ketoprofen (KET) was used
Available online 20 June 2014 (3 mg/kg BW) intramuscularly for three consecutive days post-partum (p.p.) on 19 sows.
Nineteen sows were used as a control group and they received sodium chloride as placebo
Keywords: (PLAC). All 38 sows were videotaped for 3 days p.p., in total of 6 h a day for behavioural analy-
Behaviour sis. Percentages, bout lengths and numbers of occasions were calculated from four different
Farrowing
body postures (standing, lateral and sternal lying and lying udder towards piglet area, UTP)
Pain
and active head movements. Numbers of all nursings and percentages of unsuccessful and
Sow
Ketoprofen sow terminated nursings were calculated. Feeding and drinking were observed as numbers
of occasions. Differences between treatments (KET and PLAC) and parities (young, parity
2–3 and old, parity 4–9) were analyzed with repeated measures mixed models. No treat-
ment effect was detected on any measured parameter. Interactions between treatment
and parity were found for position changes, standing, feeding, drinking and UTP (P < 0.05
for all). Young KET sows presented more position changes than young PLAC sows (29.3 ± 3.0
vs. 20.1 ± 3.0, P = 0.04) and more standing bouts than old KET ones (2.6 ± 0.4 vs. 0.9 ± 0.4,
P = 0.03). Young KET sows had more UTP bouts than PLAC peers (4.1 ± 0.4 vs. 2.3 ± 0.4,
P = 0.05). Old KET sows drunk less often than PLAC peers (0.6 ± 0.3 vs. 1.5 ± 0.3, P < 0.01)
but young KET sows ate more often than old KET sows (2.3 ± 0.4 vs. 1.0 ± 0.3, P = 0.01).
Young sows in general appeared more active and they were changing position more fre-
quently than old KET sows. In conclusion, lying passively may be one of the signs of pain
after farrowing in young sows and when treated with ketoprofen, they exhibit increase of
movement.
© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Farrowing is intrinsically a painful process, but very


little is known about pain that sows might experience post-
farrowing. Before farrowing sow behaviour is characterized
by increased activity (Jarvis et al., 2001) and the onset of
∗ Corresponding author at: Department of Production Animal
lactation turns her rapidly into lateral lying that appears
Medicine, Koetilantie 7, P.O. Box 57, 00014 University of Helsinki, Finland.
Tel.: +358 50 4156657. as passive behaviour (Oliviero et al., 2008; Wallenbeck
E-mail address: elina.viitasaari@helsinki.fi (E. Viitasaari). et al., 2008; Malmkvist et al., 2012). Post-partum (p.p.) sows

http://dx.doi.org/10.1016/j.applanim.2014.06.005
0168-1591/© 2014 Elsevier B.V. All rights reserved.
E. Viitasaari et al. / Applied Animal Behaviour Science 158 (2014) 16–22 17

are at high risk for painful conditions. Increased lying p.p. 2.1. Animals and housing
predisposes sows to skin lesions due to roughness of the
flooring material (Norring et al., 2007). In our previous We performed a double blinded, placebo-controlled
study, we found that sows treated with ketoprofen devel- field trial with a total of 38 clinically healthy Norwegian
oped skin ulcers later during lactation than the control landrace-Yorkshire hybrid sows with parity ranging from
sows (Viitasaari et al., 2013) which may be due to reduced 2 to 9 in a commercial piglet producing farm in West-
lying. A decrease in lateral lying behaviour reduces the ern Finland. The sows were moved from group-housing
possibilities for piglets to manipulate the udder. Injuries to farrowing crates (225 cm × 72 cm) approximately 7 days
and pain in the udder caused by piglets during nursing prior to expected farrowing. The crates had fully slatted
are common (Gallois et al., 2005) and may cause inter- floors with a heat plate and a heat lamp for the piglets on
rupted sucklings leading to insufficient emptying of udder either side of the sow. Each sow received a handful of fresh
(Rutherford et al., 2011). However, the association between straw every day. Lactating sows were given commercial liq-
pain and problems in lactation are not well understood uid feed five times daily, with an initial energy content of
in sows. In addition, especially old sows may suffer from 17.6 MJ on day 1, and increasing up to 128.0 MJ by the day
chronic pain due to multifactorial conditions (Baer and 18 of lactation. Water was available ad libitum from a water
Bilkei, 2005). nipple.
Lying behaviour and position changes have been related Progress of farrowing of the sows were monitored dur-
to be part of a pain response in sows. Administration of the ing piggery working hours (from 06:00 to 15:00) and
nonsteroidal anti-inflammatory drug (NSAID) meloxicam assisted if necessary. After all piglets of each sow were
p.p. has been shown to reduce sows’ total lying duration considered to be born and placenta expulsed, piglets were
(Mainau et al., 2012). Endogenous opioids increase pain isolated from their mother with a low fence for approxi-
threshold during farrowing in sows and thus act as anal- mately 1.5 h and the sow received an injection of 7–10 IU
gesics even for up to 7 days of lactation (Jarvis et al., 1997). of oxytocin to improve colostrum excretion. Cross foster-
Sows receiving naloxone (an opioid antagonist) spent less ing was initiated during the first day of their life by merging
time lying laterally and more time lying sternally than equal sized piglets into one litter. The caretakers checked
controls. Naloxone also triggered more frequent posture each sow for all signs of disease, especially for mammary
changes after farrowing which decreased after a few days oedema, vulvar discharge and leg problems, daily from far-
to the level of controls (Jarvis et al., 1999). Frequent postural rowing to weaning.
changes are also linked to high maternal defensiveness
(Baxter et al., 2011): savaging gilts, for example, change 2.2. Medication
postures more often during the puerperium than non-
savaging gilts, and this has been suggested to be part of Sows were randomly allocated into two treatment
a more complex behaviour relating to pain (Chen et al., groups in blocks of 8 within farrowing room. Nine-
2008). Parity is an important factor when assessing post- teen sows received ketoprofen (KET) (Ketovet 100 mg/mL,
partum pain as parity seem to affect the maternal behaviour Richter Pharma AGFeldgasse 19A-4600 Wels) intramus-
of sows (Vangen et al., 2005). cularly 3 mg/kg and nineteen received equal volume of
Another typical behavioural change in relation to isotonic saline as placebo (PLAC). Treatments took place
painful conditions, is a change in feeding behaviour. A during the first 1.5 h after farrowing or latest at 6 am and
reduction in feeding behaviour has been shown to be a thereafter once a day for two consecutive days. Recordings
response to malaise (Weary et al., 2008) and does not occur started each day after treatment.
during treatment with ketoprofen p.p. in sows (Viitasaari
et al., 2013). Appetite and thus eating maintains gut 2.3. Behaviour observations
movement and therefore sows also had shorter period of
constipation during p.p. ketoprofen treatment (Viitasaari A videocamera (Foscam FI8904W, Foscam Electronics,
et al., 2013). Constipation is common in p.p sows, and can HK) was installed above each pen one to 2 days before the
cause pain and reduced production performance (Oliviero expected farrowing. Data were recorded with two frames
et al., 2009). a second and was stored to a hard drive (Blue Iris v.2.64,
Our objective was to analyze changes in the behaviour of Perspective Software Corp.). Videos were analyzed using
p.p. sows of different parity after the administration of the CowLog software (Hänninen and Pastell, 2009). Videos
non-steroidal anti-inflammatory (NSAID) drug, ketopro- were observed daily from day one until day 3 p.p. Video
fen. We hypothesized that sows receiving pain alleviation observations lasted for 6 h per day in two 3-h observation
respond to the treatment by changes in general activity and windows starting 12 h after first piglet was born (Fig. 1).
improving nursing behaviour. Head and body postures, eating and nursing behaviours
of the sows were recorded continuously from the videos.
Detailed behavioural definitions are explained in Table 1.
2. Materials and methods
3. Statistics
The experimental procedures were approved by
the National Animal Experiment Board (ESAVI-2010- The sows were divided into parity 2–3 (young, n = 17)
09747/Ym-23, PH22A) and the Finnish Medicines Agency or 4–9 (old, n = 21). From the behaviour data frequencies
(FIMEA, Vetkl-nro 03/10). for all observed behaviours were calculated. Lying udder
18 E. Viitasaari et al. / Applied Animal Behaviour Science 158 (2014) 16–22

Camera installaon Time between 8:00 – 24:00

in 3 consecuve days

12 h of no recording

3h 3h
recording recording
Farrowing

Medicaon
at 6:00-
7:00each
day

Fig. 1. The beginning of behaviour recordings of sows receiving either ketoprofen (n = 19) or placebo (n = 19) for 3 days after farrowing. Recordings and
pauses took place at the same time of day for three consecutive days.

towards piglet area (UTP) was reviewed from the videos as seconds and percentages from total observation dura-
and calculated separately as an entity of its own from all lat- tion were calculated. Successful and unsuccessful nursings,
eral lying. Any change of position was calculated from the including piglet and sow terminated ones were aggregated.
video data. For the head and body postures bout durations From these, percentage of sow terminated and unsuccess-
ful nursings were calculated. For head movements only
Table 1 active ones were analyzed. For UTP, frequencies, bout
The ethogram used in observations of sows during the first 3 days of lengths and percentages of all behaviours were calculated
lactation. separately regardless if it was on the left or right flank.
Behavioural class Behaviour Description Linear mixed models for repeated measurements were
used for analysing the differences between treatments,
Body posture Standing All 4 limbs touching
the ground days and parities in all observed behaviours. In the initial
Lateral lying One shoulder and hip models, treatment (KET or PLAC), day (1–3), parity (young
touching floor and old) and their interactions were added as fixed factors,
Sternal lying Lying sternum and sow was added as a random factor. Litter size was used
touching the ground
as a covariate for all models. Only significant interactions
Head posture Active head Moving head and/or were used for the final models and reported.
nosing around while
Litter sizes, live and dead born and piglet mortality
standing, lying or
sitting between treatment groups were tested with T-tests. The
Passive head Head still, no nosing. normality and homogeneity assumptions of the models
Sow can be standing, were checked with a normal probability plot of residu-
sitting or lying als and scatter plot with residuals against fitted values.
Eating behaviour Number of feedings Head in the trough, Mixed model results are presented as model estimates and
masticating (if visible) standard errors of means (mean ± SEM). The upper limit
Number of Snout in contact with
for the significant effect was set to P < 0.05. P-value between
drinkings the water nipple
0.05 and 0.1 was considered a tendency. All statistical anal-
Nursing Number of ≥50% of piglets yses were conducted using PASW Statistics 18.0.1 (IBM
behaviour successful nursings massaging teat
Acquires SPSS Inc., 2009).
followed by silent 15 s
of suckling and end
massage. Nursing end
when 50% of piglets 4. Results
leave the teat or end
massaging Mean litter size across all sows was 15.1 ± 0.7. An aver-
Number of ≥50% of piglets
age of 12.9 ± 0.8 piglets were born alive and 2.2 ± 0.4 born
unsuccessful massaging teat
nursings continuously without dead, while 1.2 ± 0.5 died after birth during the observing
15 s silent suckling period. No differences between treatment groups in litter
time size and piglet mortality were detected (P > 0.05). In total,
Number of sow Sow turns away from three sows needed manual assistance during farrowing,
terminated piglets and terminates
nursings nursing while ≥ 50% of
one from the placebo group and two from the ketoprofen
piglets at the teat group. No signs of disease were observed in the animals
Number of piglet Piglets terminate during the study and therefore no treatments were needed.
terminated nursing after 4 min and Handling of animals was minimal; only necessary proce-
nursings sow is lying still
dures such as cleaning the pen were performed.
E. Viitasaari et al. / Applied Animal Behaviour Science 158 (2014) 16–22 19

Table 2
Overall mean (±SE) of observed behaviours in farrowed sows (n = 38) over
3 days post-partum. Observations were made for 6 h per day. Proportions
are presented as daily percentages from 6 h observation period.

Behaviour Overall value

Number Bout length Proportion


(min) (%)

Position change 20.8 ± 1.4 – –


Active head 4.0 ± 0.4 2.9 ± 0.2 3.2 ± 0.4
movements
Lateral lying 5.4 ± 0.3 58.7 ± 3.7 69.5 ± 2.6
Lying udder towards 2.8 ± 0.2 64.0 ± 7.0 37.7 ± 2.7
piglet area
Sternal lying 4.4 ± 0.4 6.2 ± 0.7 8.4 ± 0.9
Standing 1.7 ± 0.2 4.3 ± 0.5 2.3 ± 0.4 Fig. 2. The proportion of sternal lying of sows given ketoprofen (solid line)
Feeding 1.4 ± 0.2 – – or placebo (dotted line) as percentage (y-axis) of all behaviour observed
Drinking 1.3 ± 0.1 – – for 3 days postpartum (x-axis), 6 h per day *P < 0.05.
All nursings 3.2 ± 0.2 – –
Unsuccessful nursings – – 55.6 ± 2.8
Sow terminated – – 16.4 ± 2.6 higher in young KET sows than young PLAC ones. No dif-
nursings ferences between treatments were found in old sows in
these behaviours. Only number of drinking bouts was less
(P < 0.05) in old KET sows than old PLAC ones. Young sows
The overall behaviour results are presented in Table 2. showed no difference between treatments in frequency of
KET tended to increase the frequency of sternal lying bouts drinkings.
(KET 5.1 ± 0.6 vs. PLAC 3.7 ± 0.7) and the frequency of UTP
bouts (KET 3.1 ± 0.3 vs. PLAC 2.5 ± 0.3), P < 0.1 for both. 5. Discussion
Ketoprofen had no effect on duration of lateral lying bouts
(KET 63.40 ± 5.60 min vs. PLAC 54.05 ± 4.9 min, P = 0.2) No In general, behaviour of multiparous (parity 2–9) p.p.
significant treatment effects were found in lying parame- sows changed very little after treatment with the non-
ters. steroidal anti-inflammatory drug ketoprofen. However,
Time affected nursing behaviour. Number of all nursings young and old sows showed different behavioural changes
during the 6-h daily observation period decreased from after treatment. In young (parity 2–3) sows ketoprofen
day 1 to day 3 (D1: 3.9 ± 0.4, D2: 3.3 ± 0.4, D3: 2.5 ± 0.3, increased activity as compared to placebo treated ones.
P < 0.05 between D1 and D3) and the percentage of unsuc- Increased activity was seen in young KET sows as
cessful nursings decreased over the 3-day observing period increased total number of position changes but it was not
(D1: 77.7 ± 3.5 vs. D2: 51.7 ± 3.7 vs. D3 37.3 ± 4.7, P < 0.05 observed in old KET sows. Our finding in young sows resem-
for both). Bout length of sternal lying tended to increase bled a recent one in which another NSAID, meloxicam,
over time with shorter bouts on day 1 than days 2 and 3 decreased overall lying time in farrowed sows on day 3
(D1: 4.3 ± 0.9 vs. D2: 6.7 ± 0.9 and D3: 7.7 ± 0.9, P < 0.05 for p.p. (Mainau et al., 2012). However, in contrast, ibupro-
both). No other differences between days were detected. fen (NSAID) administered orally had no effect on posture
Parity affected the measured behaviour parameters changes in sows after farrowing (Lay and Haussmann,
(Table 3). In general, young sows were more active than 1999). Sows in early p.p. stage increased activity is a
old ones. preferred behavioural feature. Frequent posture changes
Several significant interactions were detected between are linked to high maternal defensiveness (Baxter et al.,
treatment and parity (Table 4). Old KET sows had longer 2011) which is an important factor in protecting the young
active head movement bouts than did young KET sows, in the wild (Mignon-Grasteau et al., 2005). In addition,
whereas young PLAC sows had longer active head move- low activity level soon after farrowing is associated with
ment bouts than young KET sows (P < 0.05). Young KET high piglet mortality (Valros et al., 2003). On the other
sows had more position changes, standing bouts, sternal hand, Haussmann et al. (1999) found a decrease in posture
and lateral lying bouts and higher feeding frequency than changes on day 3 post-partum after administering butor-
did old KET and young PLAC sows (P < 0.05). Old KET sows phanol tartrate (an opioid analgesic) in comparison to a
had less drinking bouts than young KET and old PLAC sows placebo treatment. This contrasting result might be due to
(P < 0.05). Young KET sows had higher feeding frequency that we compared sows of a different age range and that
than did old KET and young PLAC sows (P < 0.05). the drug, butorphanol tatrate, used by Haussmann et al.
The only interaction between treatment and day was (1999) affects the central nervous system. It is possible that
detected in proportion of sternal lying (Fig. 2), which was in our study young sows experienced pain after farrow-
on day 2 higher in KET sows than PLAC ones (P < 0.05). ing and when it was alleviated, they exhibited improved
Significant differences were detected between treat- maternal characteristics. If, on the other hand, the increase
ments within parity as follows: active head movement bout in activity level is due to negative motivators, such as fear, it
length was shorter in young KET sows than young PLAC might not be positive for the maternal abilities. It has been
ones. Numbers of position changes, standing bouts, ster- shown that human presence can increase sow mobility,
nal lying bouts, lateral lying bouts, feeding and UTP were leading to crushing of piglets (Lensink et al., 2009). In our
20 E. Viitasaari et al. / Applied Animal Behaviour Science 158 (2014) 16–22

Table 3
Effect of parity on mean observed (±SE) behaviours over 3 days post-partum. Observations were made for 6 h per day.

Parity behaviour 2–3 (n = 17) 4–9 (n = 21) P

Number of position change 24.7 ± 2.1 16.9 ± 1.9 <0.05


Number of active head movements 5.0 ± 0.6 3.1 ± 0.5 <0.05
Number of lateral lying 6.6 ± 0.5 4.2 ± 0.5 <0.05
Duration of lateral lying bout (min) 50.5 ± 5.0 67.0 ± 5.4 <0.05
Number of lateral lying udder towards piglet area 3.2 ± 0.3 2.4 ± 0.3 <0.05
Duration of lateral lying udder towards piglet area bout (min) 43.1 ± 10.1 85.0 ± 9.6 <0.05

study, human interaction was minimal, limited mainly to feedings, and feeding behaviour has been explained to
drug administration, and we did not differentiate observa- be a useful indicator to follow when suspecting painful
tions with or without human interaction. Old sows had no conditions (Weary et al., 2008). Energy demand increases
such reaction to ketoprofen and were in general less active as lactation proceeds (for review, see Algers and Uvnäs-
than young sows. In old sows ketoprofen might not be Moberg, 2007) and thus maintaining good feeding capacity
able to alleviate underlying multifactorial pain and inflam- is of great importance. Pain and sickness are at least
matory stages arising from previous clinical or subclinical partly mediated by the same mediators (Bay-Richter et al.,
mammary gland problems that can only be seen in ultra- 2011; Alexander et al., 2012) and may trigger same kind
sonography (Baer and Bilkei, 2005). Marchant and Broom of behaviours. Consequently feeding behaviour decreases
(1996) suggested that discomfort in dry sows increases during sickness (Weary et al., 2008) and hence pain and
standing and sternal lying. And it is possible that physi- sickness are tightly linked and might be problematic to
cal discomfort may influence posture changes post-partum discriminate.
too. In addition to increased feeding frequency, drinking
General activity in young sows, independent of treat- frequency was increased in KET young sows in compari-
ment, was higher than in old sows. Young sows showed son to young PLAC sows. Feeding and drinking have been
more position changes and shorter and more frequent described to have joined actions in the pain and sickness
bouts of lateral lying than old sows during the first 3 days responses, and usually both decrease as a response to
of lactation. This supported the finding of Mainau et al. pain (Watkins and Maier, 1999) This is further supported
(2010) that activity level is higher in primiparous than by the findings by Arras et al. (2007) that NSAID treat-
multiparous sows before and during farrowing. Our results ment after laparotomy increased the water intake in mice.
showed that this difference of activity was maintained also Even though we found no effect of ketoprofen on nurs-
during the first days of lactation. Age tends to decrease ing behaviour, an increase in water intake can potentially
general activity in sows. In addition to reduction in mater- increase milk production. High water intake during lacta-
nal reactivity with increasing parity (Held et al., 2006), a tion has been shown to correlate positively with weaning
decrease in postural changes comparing parities 1, 3 and 5 weight of the piglets and relative weight loss of the sow
are also found (Ostović et al., 2012). These previous find- during lactation (Kruse et al., 2011). Since high water intake
ings reinforce our results of general depression in maternal has a positive impact on piglets and ketoprofen increased
behaviour with increasing age. number of drinking bouts, nutritional activities should not
Young sows ate more frequently after farrowing when have a negative impact on nursing behaviour in terms of
receiving ketoprofen than placebo. This was in line with our standing position of the sow while feeding or drinking.
previous findings indicating that ketoprofen after farrow- Ketoprofen treated sows spent proportionally more
ing improved the appetite of sows (Viitasaari et al., 2013). time lying sternal on day 2 p.p. than placebo treated ones.
Hence the effect of ketoprofen was beneficial. Reduced This might have been due to reduced udder soreness in
feeding frequency in young sows was probably a sign of ketoprofen sows. Lying sternally has been suggested as
underlying pain, since ketoprofen increased number of a normal way for crated sows to limit udder stimulation

Table 4
Mean observed (±SE) behaviours over 3 days post-partum in farrowed sows of different parities (n = 38) treated either with ketoprofen or placebo. P-values
are presented as between parities within treatments. Observations were made for 6 h per day.

Parity behaviour Treatments and parities

Ketoprofen P Placebo P

2–3 (n = 9) 4–9 (n = 10) 2–3 (n = 8) 4–9 (n = 11)

Active head movement bout (min) 1.6 ± 0.5 3.5 ± 0.5 <0.05 3.7 ± 0.5 2.7 ± 0.4 NS
Number of position changes 29.3 ± 3.0 13.4 ± 2.7 <0.05 20.1 ± 3.0 20.4 ± 2.6 NS
Number of standing bouts 2.6 ± 0.4 0.9 ± 0.4 <0.05 1.3 ± 0.4 1.9 ± 0.4 NS
Number of sternal lying bouts 7.0 ± 0.9 3.1 ± 0.8 <0.05 3.1 ± 0.9 4.3 ± 0.7 NS
Number of lateral lying bouts 7.7 ± 0.7 3.5 ± 0.7 <0.05 5.5 ± 0.7 4.8 ± 0.6 NS
Number of drinking 1.6 ± 0.3 0.6 ± 0.3 <0.05 1.3 ± 0.3 1.5 ± 0.3 NS
Number of feeding 2.3 ± 0.4 1.0 ± 0.3 <0.05 1.1 ± 0.4 1.3 ± 0.3 NS
Number of lateral lying bouts udder towards piglet area 4.1 ± 0.4 2.2 ± 0.4 <0.05 2.3 ± 0.4 2.6 ± 0.4 NS
E. Viitasaari et al. / Applied Animal Behaviour Science 158 (2014) 16–22 21

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6. Conclusions
Jarvis, S., McLean, K.A., Calvert, S.K., Deans, L.A., Chirnside, J., Lawrence,
A.B., 1999. The responsiveness of sows to their piglets in relation to
Ketoprofen influenced some behavioural patterns in the length of parturition and the involvement of endogenous opioids.
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