Published December 5, 2014

Improving adaptation to weaning: Effect of intermittent suckling

1
regimens on piglet feed intake, growth, and gut characteristics
M. Berkeveld,*2,3 P. Langendijk,4 N. M. Soede, B. Kemp, M. A. M.
Taverne,* J. H. M. Verheijden,* N. Kuijken, and A. P. Koets*
*Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Yalelaan
7,
3584 CL Utrecht, the Netherlands; Adaptation Physiology, Animal Sciences Group,
and Research Farm Sterksel, Animal Sciences Group, Wageningen University,
PO Box 336, 6700 AH Wageningen, the Netherlands
ABSTRACT: Daily separation of sows and piglets
during lactation, intermittent suckling (IS), improves
feed intake and postweaning adaptation in piglets. The
aim of the current study was to determine how, in piglets that have been subjected to IS, age at weaning
and the duration of the preceding IS period contribute
to postweaning adaptation through effects on feed intake, growth, and gut characteristics. All piglets had
ad libitum access to creep feed from d 7. Litters were
subjected to conventional weaning (CW) or to 1 of 3 IS
regimens. In CW, litters (n = 29) had continuous access to the sow until weaning (d 26, d 0 = farrowing).
During IS, litters had access to the sow between 1600
and 0600 h. Litters in the IS treatments were subjected
to IS 1) from d 19 onward and weaned at d 26 (IS19
7D, n = 33), 2) from d 19 onward and weaned at d
33 (IS1914D, n = 28), or 3) from d 26 onward and
weaned at d 33 (IS267D, n = 33). The IS197D regimen resulted in a relative growth check within the first
2 d after weaning similar to CW litters (72 13 and 90
7%, respectively), but in a greater piglet growth (P
= 0.014) and feed intake (P = 0.001) between d 2 and
7 postweaning. Moreover, IS197D was not associated
with a (further) reduction in villus height as observed
at d 2 postweaning in CW litters. In IS piglets weaned
after an extended lactation (d 33), a markedly smaller
weaning-associated relative growth check was observed

shortly postweaning (11 18 and 32 19% for IS19

14D and IS267D litters, respectively). In these litters,
feed intake and growth within the first 2 d after weaning were slightly greater when piglets were subjected to
IS for 2 wk (IS1914D) rather than for 1 wk (IS267D;
P = 0.032 and P = 0.037 for feed intake and growth,
respectively). Irrespective of duration of IS, weaning at
d 33 with IS was not associated with a reduction in villus height. Irrespective of treatment, plasma citrulline
concentrations were reduced at d 2 and 8 postweaning
compared with the values at weaning (P 0.01). No
correlation was observed between postweaning plasma
citrulline concentrations and postweaning small intestinal villus height. This study indicates that 1 wk of IS
before weaning at d 26 of lactation improves feed intake
and growth between d 2 and 7 postweaning and does
not result in a reduction of villus height as observed
in CW piglets, although it did not prevent a profound
growth check shortly after weaning. However, combining 1 wk of IS with an extended lactation improved
postweaning adaptation markedly in terms of growth,
feed intake, and gut characteristics. Increasing the duration of IS from 1 to 2 wk slightly improved growth
and feed intake shortly after weaning, but the contribution to postweaning adaptation seemed to be relatively
small compared with extending lactation.

Key words: citrulline, intermittent suckling, intestinal morphology, pig, weaning

2009 American Society of Animal Science. All rights reserved.

The authors thank the personnel of the Sterksel research farm

(Sterksel, the Netherlands), and all Master of Science students for
their technical assistance, and Gisabeth Binnendijk (Animal Sciences Group, Wageningen University and Research Centre, Lelystad,
the Netherlands) for her help with the data management system.
Furthermore, we gratefully acknowledge Andrea Grne (Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Utrecht,
the Netherlands) for her helpful suggestions on the histological
proce- dures and the use of image analyses facilities, and Margriet
Hendriks and Monique de Sain (Department of Metabolic and
Endocrine Dis-

J. Anim. Sci. 2009. 87:3156

3166 doi:10.2527/jas.20081764

eases, University Medical Center Utrecht, Utrecht, the Netherlands)

for the plasma citrulline analysis.
2
Current affiliation: Danone Research BV, Wageningen, the Netherlands.
3
Corresponding author: marieke.abrahamse@danone.com
4
Current affiliation: SARDI Livestock Systems, University of Adelaide, Roseworthy Campus, SA 5371, Australia.
Received December 24, 2008.
Accepted June 23, 2009.

3156

2
sows [TOPIGS20 (Landrace York), TOPIGS, Helvoirt, the Netherlands] and their litters with an average
parity of 3.5 0.1 (ranging from 1 to 9) were used.
The numbers of sows used in replicates 1 to 4 were 29,
33, 29 and 33, respectively. Piglets were TOPIGS20
TEMPO crossbreds (TOPIGS). One week before farrowing, pregnant sows were individually housed in a
farrowing pen (2.4 1.8 m) with farrowing crate. An
infrared heated area was provided for the piglets from
birth until d 14. Artificial lighting was provided between 0600 and 1800 h and was dimmed during the
night. At weaning, each litter was moved from their
farrowing pen to its own nursery pen (1.77 2.65 m).
Litters remained in the nursery pen until the end of the
experiment (d 61).
Litter size was standardized within 2 d after farrowing by cross fostering, resulting in an average litter size
of 12.4 0.1 piglets. One day after farrowing, piglets
were weighed and received an eartag for individual identification. Within 1 wk after farrowing, piglets received
a 1-mL (200 mg) intramuscular iron injection (Prevan
200, Eurovet Animal Health, Bladel, the Netherlands).
Within each replicate, the beginning of the experimental procedure (d 0) was designated as the day at which
most of the litters were born. Litters were born from 3
d before to 3 d after d 0, and piglet age at d 0 was 0.4
0.2 on average.
All litters were offered ad libitum access to creep feed
from d 7 onward. From d 7 to 12, a 1:1 mix of 2 commercial creep feed diets was offered in a feeding bowl
(diet 1, 19% CP, 1.1% lysine, Babito, Havens Voeders, Maashees, the Netherlands; diet 2, 16.1% CP, 1.2%
lysine, Almido Big, Havens Graanhandel NV). From d
12 until d 40, diet 2 was offered in a piglet feeder with
2 feeding places (15 cm/feeding place). From d 42 until
the end of the experiment (d 61), a commercial creep
feed for weaner pigs (diet 3; 17.1% CP, 1.15% lysine;
Havo Opfok Sprint, Havens Voeders) was offered. During a 2-d transition period (d 40 to 42), diets 2 and 3
were mixed (1:1) for a gradual transition. During the
entire experiment, drinking water was continuously
available, provided by 1 drinking nipple per pen. Sows
were fed an increasing amount of feed (Euro
Airline Lactokorrel, 15% CP, 5.1% lysine, Cehave
Landbouw- belang Voeders, Veghel, the Netherlands)
after farrow- ing until the maximum allowance of 7.5
kg was reached at d 13 of lactation.

Adaptation to weaning
by et
intermittent
suckling
Berkeveld
al.

INTRODUCTION
Conventional weaning of piglets is associated with a
reduced postweaning nutrient intake, reduced growth,
and a greater susceptibility to diarrhea. Intermittent
suckling (IS), a management strategy in which sow
and piglets are separated during a fixed period of the
day, stimulates preweaning creep feed intake and, as a
result, improves postweaning feed intake and growth
(IS from d 14, weaned at d 25; Kuller et al., 2004).
Moreover, combining IS with an extended lactation
period improved adaptation to weaning, as judged by
the markedly reduced postweaning growth check and
greater feed intake after weaning (Berkeveld et al.,
2007b). Average feed intake during the first week of IS
is less when 14-d-old piglets are subjected to IS, but
is markedly increased when piglets are 1 wk older at
initiation of IS (Berkeveld, 2008). One may question
whether postponing the onset of IS to an older age,
together with the associated greater feed intake, facilitates the adaptation to weaning. However, in the latter
study, initiation of IS at a later age coincided with a
later weaning age as well, making it hard to evaluate
the relative contribution of weaning age and age at the
start of IS. Moreover, no comparison was made to a
conventional weaning (CW) regimen.
A 2-wk period of IS before weaning reduced the weaning-associated villus atrophy and increased postweaning
small intestinal (SI) absorption, if creep feed was provided (Nabuurs et al., 1996); no data on piglet feed intake or piglet growth were presented. Recent IS studies
focused on the effects of IS on piglet growth and feed
intake (Kuller et al., 2007; Millet et al., 2008). Hence,
the effect of IS regimens on postweaning SI variables,
and the relation of these variables with feed intake and
growth, remain to be elucidated.
The aim of the current study was to determine how
age at weaning in piglets that have been subjected to
IS, and the duration of the preceding IS period, each
contribute to postweaning adaptation through effects
on feed intake, growth, and gut characteristics. Besides
macroscopic and morphologic variables of the small
intestine, plasma citrulline concentration, a possible
marker for SI function (Berkeveld et al., 2008), and its
relation to SI morphology were determined.

MATERIALS AND METHODS

The Ethics Committee for animal experiments of
Wageningen University and Research Centre approved
the experimental design, including all procedures involving animals.

Animals, Housing, and Diet

The experiment was conducted in 4 replicates between April and November 2007 at the Sterksel research farm (Animal Sciences Group, Sterksel, the
Netherlands). During these 4 replicates, a total of 124

Treatment
s
Within each replicate, sows were allocated to treatments based on sow parity and BW 1 wk before farrowing. The sow and her litter were subjected to CW or to
1 of 3 IS regimens (Figure 1). Litters receiving different
treatments were housed in separate similar farrowing
rooms to prevent possible disturbing effects of nursing
litters in the same room, whereas other litters were separated from their sow during IS. In CW litters (n =
29), piglets had continuous access to the sow until
weaning

Figure 1. Schematic presentation of the interventions within each treatment. CF = start of creep feed (d 7); IS = onset of intermittent
suck- ling; W = weaning. Shaded bars indicate period of IS. CW = conventional weaning at d 26; IS197D = IS from d 19, weaning at d 26;
IS1914D
= IS from d 19, weaning at d 33; IS267D = IS from d 26, weaning at d 33.

at d 26. In the IS treatments, litters had continuous

access to the sow until subjected to IS. Litters in the
IS treatments were 1) subjected to IS from d 19 and
weaned at d 26 (IS197D, n = 33); 2) subjected to IS
from d 19 and weaned at d 33 (IS1914D, n = 28); or
3) subjected to IS from d 26 and weaned at d 33 (IS26
7D, n = 33). During IS, sows were separated from their
litter for 10 h/d (from 0600 until 1600 h) and housed
individually in a different room to prevent visual and
auditory contact. Only during absence of the sow, an
infrared light provided heating for the piglets. Litters
in the IS197D and CW treatments were weaned at d
26, and those in the IS1914D and IS267D treatments
were weaned after lactation was extended for 1 wk (d
33). Piglets were weighed at 1 d after farrowing, and at
d 19, 21, 26, 28, 33, 40 and 61. Litters weaned at d 33
(IS1914D and IS267D) had an additional weighing
at d 35. Creep feed residuals per litter were determined
simultaneously with the weighing of the piglets.

Collection of Samples
A total of 10 litters per treatment of the first 2 replicates were selected on d 25 based on litter feed intake
(closest to treatment average). Within each of these litters, 3 piglets were selected based on their BW (closest
to litter average), resulting in a total of 30 piglets per
treatment (n = 120 piglets in total). The 3 piglets per
litter were killed at weaning, or at d 2 and 8 postweaning, respectively, by intracardial injection of Euthesate
(0.75 to 1 mL/kg of BW; Ceva Sant Animale, Naaldwijk, the Netherlands) after a 5-mL cardiac blood sample was obtained. The blood sample was transferred
to a heparin-coated tube, and after centrifugation (10
min, 2,000 g at 4C), plasma samples were stored
at 80C. The abdominal cavity was opened, and gut
segments (3 cm) for microscopy were obtained at ~10,
~50, and ~90% of the SI length (duodenal, jejunal,
and ileal sections). The gut segments were opened
lengthwise and pinned on a piece of dental wax with

the serosal side to the wax. Subsequently, the samples

were fixed in 4% formalin solution with the mucosal
side downwards to fix the villi vertically. The entire
small intestine was dissected from the remaining mesentery, and the length and weight were determined. In
the first replicate, SI weight was only determined with
its contents. In the second replicate, the weight of the
emptied small intestine was also determined (n = 5 per
treatment). In both replicates, the large intestine (LI)
was isolated, and the weight was determined, with and
without its contents.

Histological
Procedure
Two transverse tissue samples were cut from each
segment using a stereo microscope. These parts of the
tissue sample were dehydrated, embedded together in
paraffin wax, and sectioned at 4 (or 5) m. One section
was transferred to a slide and stained with hematoxylin and eosin. Hence, each slide contained 2 transverse
tissue samples of a gut segment. In each slide, villus
height and crypt depth were determined for at least 10
villi and crypts (17.4 0.2 observations per slide on
average) using an image analysis system with a monitor
(Image Tool version 3.0, UTHSCSA Dental Diagnostic
Science, San Antonio, TX). Villi and crypts were only
measured when there was a complete longitudinal section of a villus and an associated crypt. The average
villus height and crypt depth per slide was used as experimental observation.

Plasma
Concentration

Citrulline

Plasma citrulline concentrations obtained before euthanization of the piglets were analyzed by automated ion-exchange chromatography performed on a Jeol
Amino-Tac (JLC-500/V, Tokyo, Japan) with postcolumn ninhydrin derivatization (Berkeveld et al., 2008).

The detection range was from 3 to 1,000 M, with a

maximal inaccuracy of 14%.

Calculations
Cumulative feed intake at each weighing was calculated by summing the total feed intake at all previous times of weighing. A relative growth check was
defined as the reduction in ADG in the first 2 d after
weaning, from d 26 to 28 for IS197D and CW litters,
and from d 33 to 35 for IS1914D and IS267D litters, compared with the ADG in the last 5 d before
weaning, and expressed as a percentage. The relative
growth check (%) was calculated as 100(ADGd 2126
ADGd 2628)/ADGd 2126 for litters weaned at d 26 and
as 100(ADGd 2833 ADGd 3335)/ADGd 2833 for litters
weaned at d 33.

Statistical
Analysis
Data are presented as means SE. Normally distributed data were analyzed using the MIXED procedure
(SAS Inst. Inc., Cary, NC). Litters were individually
housed in a separate farrowing pen and, hence, considered as the experimental unit. In each replicate, the 7
to 9 pens (= litters) of 1 treatment were located in
1 of the 4 very similar farrowing rooms. The
experiment was conducted during 4 replicates, and
each
replicate contained all
4 treatments. As
mentioned previously, the different farrowing room
per
treatment was
used to prevent
possible
disturbing effects of nursing litters in the room,
whereas other litters were separated from their sows.
The applied experimental design did not include a
treatment group with an extended lactation (weaning
at d 33) without IS. This means that only pair-wise
comparisons were made between litters weaned at d
26 (CW vs. IS197D) or those at d 33 (IS1914D vs.
IS267D), or between litters with 1 wk of IS weaned at
d 26 or 33 (IS197D vs. IS267D). Moreover, we want
to emphasize that possible treatment effects in litters
weaned at d 33 cannot be entirely contributed to age at
weaning or IS alone.
Although litter was the experimental unit for ADFI,
ADG, and BW, and used as such in statistical analyses, all data were expressed per piglet. Effects were
considered significant when P < 0.05; in posthoc testing the Bonferroni correction was applied. Correlations
were
calculated using
Pearson
correlation
coefficients of SAS.
Because feed intake data of the first 3 wk (until d
21) were not normally distributed, they were analyzed
using PROC NPAR1WAY, a nonparametric KruskalWallis test. If this test detected an overall treatment
effect, data of treatments were tested pairwise. Feed
intake data (from d 26 onward), BW, and ADG were
analyzed as litter characteristics with treatment as
fixed factor, replicate and sow as random factors, and
age at d 0, BW at d 19, litter size (only for feed intake)

and sow parity as co-variables. Body weight at d 19

was omitted as co-variable from the model for analysis

on piglet birth weight and replaced by birth weight for

analysis on mean litter ADG and BW at d 19.
Data on intestinal macroscopic variables, plasma citrulline concentration, and intestinal morphology (villus
height and crypt depth) were analyzed with treatment,
day, and sex as fixed factors, sow and replicate as random factors, and age at d 0 and BW at d 19 as co-variables. Only during analysis of intestinal macroscopic
variables, the effect of the interaction of treatment and
day was significant in several cases and therefore
add- ed to the model. For analysis of intestinal
morphology data, sampling location (duodenum,
jejunum, and il- eum section) was added as a fixed
factor to the model. Measurements on villus height
and crypt depth at the 3 sampling locations
(duodenal, jejunal, and ileal sections) were averaged
per piglet. These average val- ues were used to present
data on villus height and crypt depth per treatment
and to relate intestinal morphol- ogy to other
variables obtained in the study (such as
piglet growth and plasma citrulline).

RESULTS
Feed
Intake
Creep feed intake before d 19 was negligible for all
treatments. Between d 19 and 26, IS197D and IS19
14D litters were subjected to IS, whereas CW and
IS267D litters were still continuously suckled. Feed in-

take of litters subjected to IS in this period (d 19 to 26)

was still small, however, and did not differ from that
of the continuously suckled CW and IS267D litters
(Table 1). At d 26 both CW and IS197D litters were
weaned, whereas the 2 other treatments (IS1914D and
IS267D) were weaned 1 wk later at d 33. Weaning (d
26) markedly increased feed intake in CW and IS19
7D litters compared with the unweaned IS1914D and
IS267D litters, both during the first 2 d after weaning
and from d 28 to 33. In the first 2 d after weaning, feed
intake did not differ between litters weaned at d 26, but
feed intake between d 28 and 33 was greater in IS197D
litters compared with CW litters (P = 0.001).
In litters with extended lactation (weaning at d 33),
no differences in feed intake were observed between
IS1914D and IS267D treatments during the suckling
period. However, in the first 2 d after weaning feed
intake was greater for litters subjected to 14 d of IS as
compared with litters subjected to 7 d of IS (P = 0.032;
Table 1). Thereafter, feed intake of both treatments
was similar. Between d 35 and 40, feed intake of litters
weaned at d 33 was less than that of litters weaned 1
wk earlier (P < 0.012; Table 1). During the last 3 wk of
the experiment (d 40 to 61), feed intake was still greater for IS197D litters than for IS1914D and IS267D
litters (P < 0.007) and also greater in CW compared
with IS267D litters (P = 0.003; Table 1).
In all treatments, cumulative feed intake during lactation (Table 1) was correlated to feed intake in the
first 2 d postweaning (r > 0.57; P < 0.002). At the end

Table 1. Feed intake of piglets per treatment during lactation and after weaning (W)
Treatment
Day1

Item
3

ADFI, gpiglet d

19 to 21
21 to 26
26 to 28
28 to 33
33 to 35
35 to 404
40 to 61
12 to W, g/piglet
12 to 61, kg/piglet

CUMFI5

CW

IS197D

IS1914D

IS267D

72
14 3
a
103 7*
a
164 9

362 13a
ab
808 21
103 2a
a
20.6 0.5

51
19 3
a
112 9*
b
203 9

375 15a
b
829 21
126 2ab
a
21.4 0.6

51
20 4
b
37 5
75 10c
a
244 17*
325 12b
ac
775 19
587 8c
b
18.7 0.5

7 1
20 3
b
34 6
55 6c
b
201 14*
322 16b
c
752 24
484 6bc
b
18.7 0.6

ac

Within a row, means without a common superscript letter differ (P < 0.05).
Day = day of the experiment; d 0 = day on which most of the litters were born, litters were born from 3 d before to 3 d after d 0.
2
CW = conventional weaning at d 26 (n = 29); IS = intermittent suckling; IS197D = IS from d 19, weaning at d 26 (n = 33); IS1914D =
IS
from d 19, weaning at d 33 (n = 28); IS267D = IS from d 26, weaning at d 33 (n = 33).
3
ADFI (g/d) per piglet in the indicated period.
4
Because feed residuals were not determined in the CW and IS197D litters on d 35, the ADFI was calculated between d 33 and 40.
5
CUMFI = average cumulative feed intake (g or kg) per piglet in the indicated period.
1

of the experiment, cumulative feed intake of IS litters

weaned after extended lactation (IS1914D and IS26
7D) was less than for litters weaned at d 26 (CW and
IS197D; P < 0.002; Table 1).

ling (starting at d 19) resulted in a reduced growth in

IS197D and IS1914D litters between d 19 and 21,
and between d 21 and 26 of lactation when compared
with that of the continuously suckled CW and IS26
7D litters in these periods (P < 0.001; Figure 2). This
reduced growth after onset of IS resulted in a lighter
BW for IS197D and IS1914D litters at d 21 and 26
compared with CW and IS267D litters (P < 0.001;
Table 2). Weaning (d 26) resulted in a dramatic decrease in piglet growth in IS197D and CW litters (Figure 2), with a relative growth check of 72 13 and 90
7%, respectively (P > 0.05). However, piglet growth
between d 2 and 7 postweaning was greater for IS197D
litters than for CW litters (P = 0.014; Figure 2; d 28
to 33). The reduced growth after weaning resulted in a
lighter BW for IS197D and CW litters at d 33 compared with the intermittently suckled IS1914D and
IS267D litters (P < 0.0001).

Piglet
Performance
Piglet mortality up to d 19, before onset of treatments, was 9%. Piglet loss from d 19 until the end of
the experiment (d 61) was similar in all treatments (3.4
0.2% on average).
Piglet BW at the start of treatments (d 19) was
slightly greater in IS267D litters compared with IS19
7D litters (P = 0.026); CW and IS1914D litters were
intermediate (Table 2). Therefore, treatment effects on
BW and ADG were always corrected for BW at d 19
(see Statistical Analysis section). Intermittent suck-

Table 2. Body weight of piglets (kg) during lactation and after weaning
Treatment2
Day

0
19
21
26
28
33
35
40
61

CW
1.41
6.22
6.80
8.16
8.15
8.68

0.04
ab
0.14
0.15a
a
0.19
0.18*a
a
0.19

10.54 0.25a
21.28 0.47
ac

IS197D
1.41
6.00
6.44
7.50
7.54
8.33

0.03
a
0.14
0.14b
b
0.16
0.16*b
a
0.19

10.23 0.25a
21.48 0.53

IS1914D
1.38
6.16
6.58
7.68
8.21
9.50
9.86
11.03
21.52

0.04
ab
0.17
0.18b
b
0.20
0.21a
b
0.24
0.26*
0.27b
0.47

IS267D
1.42
6.35
6.80
8.12
8.66
9.84
10.06
11.30
21.72

0.04
b
0.13
0.14a
a
0.15
0.16c
b
0.19
0.21*
0.24b
0.47

Within a row, means without a common superscript letter differ (P < 0.05).
Day = day of the experiment; d 0 = day on which most of the litters were born, litters were born from 3 d
before to 3 d after d 0.
2
CW = conventional weaning at d 26 (n = 29); IS = intermittent suckling; IS197D = IS from d 19,
wean- ing at d 26 (n = 33); IS1914D = IS from d 19, weaning at d 33 (n = 28); IS267D = IS from d 26,
weaning at d 33 (n = 33).
*Indicates the first weighing after weaning.
1

Figure 2. Average daily gain of piglets (gpiglet1d1) during lactation and after weaning at d 26 (left graph) or at d 33 (right graph). acData
on piglet growth is presented in 2 graphs according to weaning age (d 26 or 33). However, the model used for statistical analysis of piglet growth
included all 4 treatments. Thus, at each experimental day, differences between the 4 treatments (P < 0.05) are indicated with different
letters. For instance, growth in weaned litters (CW and IS197D) between d 26 and 28 is less compared with that of unweaned litters (IS19
14D and IS267D). CW = conventional weaning at d 26 (; n = 29; left graph); IS = intermittent suckling; IS197D = IS from d 19, weaning
at d 26 (;
n = 33; left graph); IS1914D = IS from d 19, weaning at d 33 (; n = 28; right graph); IS267D = IS from d 26, weaning at d 33 (; n = 33;
right graph).

Weaning after extended lactation (d 33) also reduced

piglet growth, more so for litters subjected to 1 wk of
IS (IS267D) than for litters with 2 wk of IS before
weaning (IS1914D; P = 0.037; Figure 2). However,
the relative postweaning growth check was markedly
reduced after an extended lactation compared with the
earlier weaned IS197D and CW litters (P < 0.05): 11
18% in IS1914D and 32 19% in IS267D litters.
During the last 3 wk of the experiment (d 40 to 61),
piglet growth was greater for IS197D than for IS267D
litters (536 16 and 481 18 g/piglet/d, respectively;
P = 0.009); CW and IS1914D litters were intermediate (512 16 g/piglet/d and 499 12 g/piglet/d, respectively). However, no differences in piglet BW were
observed at the end of the experiment (d 61; Table 2).
After an extended lactation, piglet growth in the
first 2 d postweaning was correlated to the cumulative
feed intake during lactation (r = 0.44 and P = 0.021
for IS1914D, and r = 0.52 and P = 0.003 for IS26
7D litters). This correlation was not observed in litters
weaned at d 26 (r = 0.31 and P = 0.102 for CW, and r
= 0.32 and P = 0.072 for IS197D litters).

Postweaning Intestinal Macroscopy

Irrespective of treatment, SI length did not change
in the first 2 d after weaning (P > 0.05), but increased
thereafter, resulting in a longer SI at d 8 postweaning
compared with d 2 postweaning (overall P < 0.001;
Table 3). The relative increase in SI length between d

2 and d 8 postweaning seemed to be greater for piglets

weaned at d 33 (~23% for IS1914D and 12% for IS26
7D) than for piglets weaned at d 26 (~6% for CW and
~7% for IS197D). Overall, CW piglets had a smaller
SI length compared with IS piglets, irrespective of IS
regime (overall P < 0.013). Small intestinal length did
not differ overall between the IS treatments.
Small intestinal empty weight was similar in all
treatments at weaning (P > 0.10). At d 8 postweaning, piglets weaned after extended lactation (IS1914D
and IS267D treatment) had a greater SI empty weight
compared with piglets weaned at d 26 (IS197D and
CW treatment; P < 0.020).
The empty weight of the LI increased after weaning in all treatments, resulting in greater values at d
2 compared with the values at weaning (overall P =
0.017) and in greater values at d 8 postweaning compared with the preceding values (overall P < 0.001).
The empty weight of the LI was greater for IS1914D
and IS267D piglets than for the earlier weaned IS19
7D and CW piglets (P <
0.001).
Cumulative feed intake during lactation was not correlated to the SI and LI empty weight in piglets weaned
at d 26 or 33. Moreover, empty weight of the SI and
LI at d 2 and 8 postweaning correlated to the feed intake in the first 2 d postweaning (overall r > 0.74, P <
0.001) and between d 2 and 7 postweaning (overall r >
0.70, P < 0.001), respectively. Only length of the SI at
d 8 postweaning was correlated to feed intake (between
d 2 and 7 postweaning; overall r = 0.50, P = 0.001).

Table 3. Gut variables at weaning and at d 2 and 8 postweaning in each treatment1

Day postweaning
Variable

P-value
2

SI length, cm

Treatment

Treatment (P < 0.001)

Day (P < 0.001)
Treatment Day (P = 0.10)

CW
656 25
596 27
631 24
IS197D
720 41
653 39
696 40
IS1914D
666 34
649 48
800 30
IS267D
696 42
689 34
771 41
SI full weight, g
Treatment (P < 0.001)
CW
283 16a
291 18a
549 19b
a
a
b
Day (P < 0.001)
IS197D
316 24
309 21
568 50
Treatment Day (P < 0.001)
IS1914D
394 24a
486 38a
814 30b
a
a
b
IS267D
377 21
477 33
863 32
3
ab
a,x
SI empty weight, g
Treatment (P < 0.001)
CW
276 17
225 13
368 19b,x
ab
a,xy
b,x
Day (P < 0.001)
IS197D
262 29
226 25
307 32
a
a,xy
Treatment Day (P < 0.01)
IS1914D
317 35
348 41
514 34b,y
a
a,y
b,y
IS267D
321 28
356 39
593 33
2
LI full weight, g
Treatment (P < 0.001)
CW
158 10
230 23
387 18
Day (P < 0.001)
IS197D
159 13
211 15
380 31
Treatment Day (P = 0.65)
IS1914D
266 23
347 34
514 25
IS267D
280 29
353 34
576 28
2
LI empty weight, g
Treatment (P < 0.001)
CW
89 6
96 7
165 8
Day (P < 0.001)
IS197D
89 8
94 6
159 11
Treatment Day (P = 0.41)
IS1914D
129 6
155 11
212 7
IS267D
132 9
152 9
228 8
a,b
Within a row, means within each treatment with a different superscript letter are significantly different (P < 0.05).
x,y
Within a column, means within each day with a different superscript letter are significantly different (P < 0.05).
1
CW = conventional weaning at d 26; IS = intermittent suckling; IS197D = IS from d 19, weaning at d 26; IS1914D = IS from d 19,
weaning at d 33; IS267D = IS from d 26, weaning at d 33.
2
Interaction between treatment and day was not significant for this variable; therefore, only overall P-values are given. SI = small intestinal; SI
length at d 8 > SI length at d 2 (overall P < 0.001). SI length of IS litters (irrespective of regimen) > SI length of CW litters (overall P <
0.02), no differences in SI length between IS regimens. Large intestine (LI) empty and full weight increase over time with d 0 < d 2 < d 8
(overall P <
0.001). The LI empty and full weight of IS1914D and IS267D litters > IS197D and CW litters (overall P < 0.001).
3
The means SE displayed for the SI empty weight were based on observations of replicate 2 (see paragraph Collection of Samples in Materials

Postweaning Intestinal Morphology

Villus height and crypt depth were different among
sample locations, with greatest values at the proximal
intestine, intermediate at the mid small intestine, and
least at the distal end of the small intestine (overall P
< 0.001; data not shown).
Weaning reduced villus height in piglets of the CW
treatment, resulting in shorter villi at d 2 postweaning
compared with the values at weaning (P = 0.009); villus
height at d 8 was intermediate (Figure 3). In contrast,
villus height at d 2 postweaning was not different from
the values observed at weaning in the IS treatments.
Moreover, at d 8 postweaning, piglets weaned after an
extended lactation (IS1914D and IS267D treatment)
had longer villi compared with CW piglets (P = 0.038
and P < 0.001; Figure 3). Irrespective of treatment,
weaning resulted in deeper crypts at d 8 postweaning
compared with values at weaning or 2 d after weaning
(overall P < 0.001; Figure 3).
Villus height and crypt depth at d 2 postweaning were
both correlated to the ADFI in the first 2 d postweaning
(overall r = 0.58, P < 0.001 and r = 0.62, P < 0.001;
Figure 4). Moreover, villus height and crypt depth at
d 2 postweaning were both correlated to the relative
growth check in the first 2 d postweaning (overall r =
0.49, P = 0.002 and r = 0.60, P < 0.001). Villus

height and crypt depth at d 8 postweaning were also

correlated to the ADFI between d 2 and 7 postweaning
(overall r = 0.59, P < 0.0001 and r = 0.53, P <
0.001, respectively). Only a weak correlation was
found for villus height at d 8 postweaning and ADG
between d 2 and 7 postweaning (overall r = 0.38, P =
0.04), but not for crypt depth.

Postweaning
Citrulline
Concentratio
n

Plasma

Weaning reduced plasma citrulline concentrations resulting in reduced concentrations on d 2 and

8 postweaning compared with the values observed at
weaning (overall P = 0.01 and P < 0.001; Figure 5).
Postweaning plasma citrulline concentrations were not
different between treatments. At weaning, plasma citrulline concentrations were negatively correlated to
crypt depth (overall r = 0.36, P = 0.022). At d 2
postweaning, plasma citrulline concentrations were
negatively correlated to crypt depth (r = 0.46, P =
0.003) and SI empty weight (r = 0.62, P = 0.004). No
correlation was observed between plasma citrulline concentration at d 2 postweaning and the relative growth
check, ADG, or ADFI during the first 2 d postweaning.
At d 8 postweaning, plasma citrulline was correlated to
SI length (r = 0.37, P = 0.017).

DISCUSSION
The aim of the current study was to determine how
age at weaning, after a period of IS, and the duration of
IS, each contribute to the prevention of the detrimental
effects on piglet performance and on gut characteristics associated with CW. In contrast to expectations,
results of the current study demonstrate that the
wean-

Figure 3. Villus height (m; upper graph) and crypt depth (m;
lower graph) in the small intestine at weaning and at 2 and 8 d
postweaning. Values are means SE, n = 10 piglets/treatment. The
measurements on villus height and crypt depth of the 3 sampling locations in the small intestine were averaged per piglet. a,bWithin each
treatment, differences between the values per day are indicated with
different letters above the bars (P < 0.05). *Different from the
value of CW treatment at that specific day (P < 0.05); **different
from the values in the CW and IS197D treatment at that specific
day (P < 0.05); ***different from the values in all other
treatments at that specific day (P < 0.05). CW = conventional
weaning at d 26; IS
= intermittent suckling; IS197D = IS from d 19, weaning at d
26; IS1914D = IS from d 19, weaning at d 33; IS267D = IS from d
26, weaning at d 33.

Figure 4. Average daily feed intake (gpiglet1d1) in the first 2

d postweaning in relation to villus height (m; upper graph; r =
0.58, P < 0.0001) and crypt depth (m; lower graph; r = 0.62, P <
0.0001) (n = 10 piglets/treatment). CW = conventional weaning at
d 26; IS
= intermittent suckling; IS197D = IS from d 19, weaning at d
26; IS1914D = IS from d 19, weaning at d 33; IS267D = IS from d
26, weaning at d 33.

Figure 5. Plasma citrulline concentration (M) per treatment in

jugular blood samples at weaning and at d 2 and 8 postweaning (n =
10 piglets/treatment). CW = conventional weaning at d 26; IS =
inter- mittent suckling; IS197D = IS from d 19, weaning at d 26;
IS1914D
= IS from d 19, weaning at d 33; IS267D = IS from d 26, weaning
at d 33.

ing-associated growth check during the first 2 d after

weaning was not prevented or reduced by 1 wk of IS before weaning (d 26). However, it did result in a greater
feed intake and piglet growth from d 2 to 7 postweaning. Moreover, there was no (further) reduction of villus
height at d 2 postweaning as observed in CW piglets.
The combination of 1 wk of IS with an extended lactation length (weaning at d 33) reduced the postweaning
check considerably compared with piglets weaned at
d 26, with or without 1 wk of IS before weaning. This
latter effect on the growth check was slightly more pronounced when IS was applied for 2 wk before weaning
at d 33. Irrespective of its duration, IS combined with
extended lactation was not associated with a significant
reduction in villus height after weaning.
Unexpectedly, subjecting litters to IS from d 19 to 26
of lactation did not stimulate their feed intake during
this period as compared with that of continuously suckled litters in the current study. Previous experiments of
our research group demonstrated a consistent stimulation of feed intake by IS during lactation, although the
level of stimulation varied considerably, even among
experiments under the same experimental conditions
(Kuller et al., 2004, 2007; Berkeveld et al., 2007b). In
the current study, sow and piglets were, for practical
reasons, separated for 10 h/d instead of the 12 h/d applied in the mentioned studies. A duration of daily sep-

aration of only 7 h was found not to be associated with

any stimulatory effects of a 2-wk period of IS (d 14 to
28) on preweaning feed intake of piglets (Millet et al.,
2008). Therefore, the 10-h separation period applied in
the current experiment may have contributed to
the lack of feed intake stimulation during lactation
after 1 wk of IS. Even though preweaning feed intake
was not stimulated by 1 wk of IS (from d 19 to 26),
growth and feed intake between d 2 and 7 postweaning
were greater for these IS litters than for CW litters.
Such an effect of IS has been observed previously in
litters with a low preweaning feed intake level (Kuller
et al., 2004). Ap- parently, IS not only influences
preweaning feed intake, but may also have another
influence causing a better postweaning performance (to
be discussed in more de- tail below).
One week of IS between d 19 and 26 did not stimulate
feed intake and resulted in less piglet ADG and lighter
BW of IS litters compared with litters still continuously
suckled at that time. Similarly, a reduced preweaning
piglet growth and weaning weight were also observed
in previous IS studies, despite the fact that preweaning feed intake in these studies was stimulated by IS
litters (Kuller et al., 2004, 2007). The preweaning dry
feed intake of IS piglets or the ability to process the
ingested dry feed might have been still too small to
compensate for the milk deficit due to the absence of
the sow. Hence, it might be that IS is associated with
similar problems as complete weaning, thereby shifting
(part of ) the weaning problems to the lactation period.
However, the growth reduction after IS is much smaller
compared with that seen in conventionally weaned piglets, and the nutrient intake is still secured by the intermittent presence of the sow (and the increasing dry
feed intake). Furthermore, one might postulate that
2 periods of slightly reduced piglet performance
(onset of IS and complete weaning) might be
advantageous with respect to disease risk and piglet
loss, compared with 1 period of severely reduced piglet
performance as observed after CW.
While 1 wk of IS before weaning at a conventional age (d 26) did not reduce the postweaning growth
check, prolongation or postponing the period of IS for 1
wk before weaning did reduce the postweaning growth
check markedly. This is in line with a previous study
(Berkeveld et al., 2007b), in which IS (d 14 onward)
combined with an extended lactation period (weaning
at 43 1 d) reduced the postweaning growth check to
14%. The shortened lactation length (from 43 to 33 d)
and duration of IS (from 4 to 1 or 2 wk) of the current
study seemed to have been equally effective in the prevention of a postweaning growth check. These positive
effects on postweaning performance cannot entirely be
ascribed to the restriction in nursing time during the
applied IS regimens. Age at weaning itself apparently
has a crucial impact on how well piglets can cope with
weaning because a severe postweaning growth check
was absent only when 1 wk of IS starting at 26 d of
age, and not when starting at 19 d of age. In addition

to increasing weaning age, subjecting piglets to an IS

regimen does facilitate their adaptation because feed
intake and growth shortly after weaning (at d 33) were
improved by a longer period of IS during lactation.
The observed values of villus height and crypt depth
in the CW piglets of the current study correspond to
previously reported values (Nabuurs et al., 1993; van
Beers-Schreurs et al., 1998). Villus height of CW piglets
was reduced by about 21% at d 2 postweaning compared with preweaning values. Similar reductions in villus height after weaning were shown to have a profound
effect on intestinal absorption values (Nabuurs et al.,
1996). Higher villi and deeper crypts were observed at
d 8 after weaning in litters with an extended lactation
combined with 1 or 2 wk of IS compared with CW
piglets, which is in line with previous findings of Nabuurs et al. (1996) that a 2-wk period of IS (8 h/d) with
supplemental feeding before weaning (at d 35) attenuates villus atrophy and improves intestinal absorption
postweaning. Because no differences in intestinal morphology were observed in the current study between
piglets weaned at a conventional age with or without 1
wk of IS, this appears to be an effect of age, rather than
of the limited suckling time. Multiple authors (Pluske
et al., 1996; van Beers-Schreurs et al., 1998), as well as
the data of the current study, have shown a positive
cor- relation between villus height and feed intake,
indicat- ing the importance of feed intake for proper
intestinal function. Therefore, the effect of age on gut
morphol- ogy seemed to be mediated by the greater
stimulation of feed intake when piglets were subjected
to IS at an older age (339 18 vs. 104 18 g/piglet in
the first wk of IS, and 2,013 94 vs. 1,239 56
g/piglet in the first wk postweaning for IS267D and
IS197D treatments, respectively).
At weaning, villus height of piglets in the CW treatment was not different from IS197D piglets. This is
in accordance with Nabuurs et al. (1993, 1996) who
showed that the supplementation of creep feed or subjecting piglets to IS (and creep feed) from 2 wk before
weaning did not affect villus height in the small intestine of piglets weaned around 32 d of age. Surprisingly,
1 wk of IS before weaning at d 26 did not result in
a significant reduction in villus height as observed in
CW piglets, despite the fact that feed intake before and
within the first 2 d after weaning was not improved
compared with the latter. Although the small sample
size in the present study could have complicated detection of a reduction in villus height after weaning, beneficial effects of IS might also be mediated by factors
other than an increased feed intake. One possible explanation could be the habituation of IS piglets to separation from their mother at the time they are weaned
permanently. An attempt to eliminate nutritional stress
at weaning by feeding piglets increased quantity of milk
from the sow attenuated, but did not completely prevent, the weaning-associated villus atrophy (van BeersSchreurs et al., 1998). Overnight maternal separation
has been found to be associated with elevated basal

cortisol concentrations in piglets (Klemcke and Pond,

1991). Moreover, weaning of 19-d-old piglets has been
shown to activate stress signaling pathways, which mediate and contribute to the intestinal dysfunction (i.e.,
increased SI permeability), associated with weaning
(Moeser et al., 2007). Therefore, piglets habituated to
repeated maternal separation in the IS regimen may
have had a reduced stress response after weaning, and
this could have prevented or attenuated intestinal damage. Although an IS regimen could result in more stress
before weaning, subjecting piglets to IS was not associated with any behavioral patterns indicative of piglet
distress (Berkeveld et al., 2007a).
The plasma citrulline concentrations of the piglets
at the day of weaning (d 26 or 33) correspond well
to the concentrations of 29-d-old suckling piglets reported previously [122 25 M; n = 7; jugular vein
sample; Flynn and Wu (1997)]. In line with previous
findings of our group (Berkeveld et al., 2008), weaning
reduced plasma citrulline concentrations. Plasma citrulline concentrations are less in human patients with
villus atrophy associated with small bowel diseases
compared with healthy subjects and are considered to
be a marker of enterocyte mass (Crenn et al., 2003).
It was therefore anticipated that the postweaning reduction in plasma citrulline concentrations would be
caused by the villus atrophy and impaired intestinal
function associated with weaning. Unexpectedly, weaning of IS and CW litters in the current study resulted in
a similar reduction of plasma citrulline concentrations,
despite the fact that IS prevented a weaning-associated
villus atrophy and resulted in a greater postweaning
feed intake. Moreover, only a few and rather weak correlations were observed between plasma citrulline and
SI morphology. Because the plasma citrulline concentration was determined in cardiac blood samples, it is
the net resultant of SI citrulline production and cellular
uptake and metabolism.
Weaning is associated with numerous changes in
the piglet environment, but one of the most important
changes is the transition from a diet consisting mainly
of milk to a nonmilk diet. Despite the fact that creep
feed intake is already substantial in IS litters during
extended lactation, the complete deprivation of milk of
the sow after weaning might possibly have altered the
metabolism of citrulline produced in the small intestine
after weaning, and thereby resulted in the decreased
plasma values, as observed after weaning in piglets of
all treatments. So, to gain more insight into the relation between SI citrulline production and morphological characteristics, a sampling location closer to the site
of citrulline production [e.g., the portal vein; Wu et al.
(1994)] would be desirable.
In European conventional pig husbandry, piglets are
weaned around 3 or 4 wk of age. As a result, weaning
is associated with a reduced nutrient intake and growth
and has a detrimental effect on intestinal structure and
function. Results of the current study demonstrate that
1 wk of IS before weaning at the conventional age (d

26) decreases weaning weight and does not prevent the

weaning-associated growth check in the first 2 d after weaning, but does result in a greater feed intake
and growth of piglets between d 2 and 7 after weaning. Moreover, it prevents a (further) reduction in villus
height as observed in CW piglets. However, postponing
the weaning age of IS piglets by 1 wk (IS267D) largely
prevented the weaning-associated growth check, indicating that age at weaning itself has a crucial impact
on how well piglets can cope with weaning. Moreover,
a longer period of IS before weaning (2 wk instead of
1 wk) at this older age improves the postweaning feed
intake and growth of piglets shortly after weaning, suggesting an even more gradual adaptation to weaning.
Similar to 1 wk of IS before weaning at a conventional
age (d 26) and irrespective of duration, villi were not
(further) shortened after weaning when IS was applied
before weaning at an older age (d 33). Despite the profound effects of IS (irrespective of regimen) on piglet
performance in the short-term postweaning period, no
differences in piglet BW were observed at the end of
the experiment. It is postulated, however, that the beneficial effects of IS on postweaning performance might
become even more pronounced (or long-lived) when
piglets are weaned under suboptimal conditions [e.g.,
at farms with a history of postweaning diarrhea (with
or without mortality)].
Although 1 wk of IS before weaning at a conventional
age (d 26) was found to have a modest, short-lasting
beneficial effect on piglet postweaning performance,
this effect was more profound when 1 wk of IS was
combined with an extended lactation (weaning at d
33). The effect of a prolonged 2-wk period of IS during
extended lactation was only limited. To conclude, we
suggest that IS combined with an extended lactation
might be a promising management strategy to improve
the adaptation of piglets to weaning. The specific contribution of age at weaning or IS to this improved adaptation remains to be elucidated.

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