Compensatory growth in the broiler

chicken: a review
A.K. ZUBAIR and S. LEESON
Department of Animal and Poultry Science, University of Guelph,
Guelph, Ontario N1G 2W1, Canada

The phenomenon of compensatory growth in broiler chickens subjected to

early life undernutrition is reviewed. Increased interest in this concept is
attributed to problems associated with early life fast growth rate, especially in
broilers fed ad libitum.These problems include high body fat deposition, and
a high incidence of skeletal and metabolic disorders. Factors that influence
compensatory growth in the broiler chicken include the nature, severity and
duration of undernutrition, as well as the age at the commencement of
undernutrition and the degree and pattern of realimentation. Many studies
have reported improvement in feed efficiency during compensatory growth in
restricted-refed broilers. Broiler chickens undergoing compensatory growth
also exhibit greater than normal feed intake relative to body weight and some
associated digestive adaptation. The use of this concept to address problems
associated with early life fast growth rate requires more studies of the nutrition
of the broiler chicken during the period of growth compensation.

Keywords: Broiler; undernutrition; compensatory growth; body fat; efficiency.

Introduction
Constant genetic selection and improvement in nutrition have led to a very fast
growth rate in modern broiler strains. Over the last 40 years the time required to
grow a broiler chicken to 2 kg body weight has decreased by about one day per
year (Portsmouth and Hand, 1987). This dramatic increase in growth rate is
manifested primarily in the first four weeks after hatching (Marks, 1979).
Unfortunately, early fast growth rate in broiler chickens is accompanied by a
number of problems - namely, increased body fat deposition, a high incidence of
metabolic diseases, high mortality, and a high incidence of skeletal diseases, e.g.
tibia1 dyschondroplasia (Leeson and Summers, 1988).
Excess body fat deposition is now of concern to both producers and consumers.
The latter consideration is important because results of many human studies have
related high dietary fat intake to the incidence of cardiovascular diseases and
cancer. High body fat deposition in broiler chickens, apart from being inefficient
0 World’s Poultry Science Association 1996
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Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
in terms of energy metabolism and overall feed utilization (Pasternak and Shalev,
19831, also represents economic loss to the producers. For example, obesity in
birds increases the incidence of reproductive failure, death due to heart failure
and impaired thermoregulation (Garlich, 1979). Most broilers are fed ad Zibifum
and the problems associated with fast growth are particularly evident under this
feeding system (Jones and Farrell, 1992a; Yu and Robinson, 1992). Ad libitum
feeding is being questioned by many workers in terms of skeletal and
cardiovascular derangements, and because of the concern over increasing adipose
hyperplasia and hypertrophy.
Many studies have demonstrated the potentials for correction of these
conditions by the use of early nutrient restriction programmes (Osbourn and
Wilson, 1960; Auckland and Morris, 1971; Plavnik and Hurwitz, 1985, 1988a,b,
1991; Jones and Farrell, 1992a,b). Accelerated (compensatory) growth results in
the body weight of birds which have been undernourished reaching, or
sometimes exceeding that of broilers fed ad libitum at market age (Plavnik and
Hurwitz, 1989, 1991; Jones and Farrell, 1992a,b).
It is essential that the effect of early age undernutrition on subsequent growth
performance and body composition changes is understood if feed restriction
programmes are to be used. This paper examines the phenomenon of compensa-
tory growth and its potential application in the broiler chicken. Results of some
recent studies of how early life feed restriction affects growth performance, feed
efficiency and body fatness in broilers are reviewed.

Concept of compensatory growth in the broiler chicken

Compensatory growth is defined as abnormally rapid growth relative to age
within a breed of animal (Bohman, 1955; Wilson and Osbourn, 1960; ODonovan,
1984). Uninterrupted growth of animals follows a predetermined growth curve.
Temporary conditions unfavourable for growth, such as undernutrition or illness,
make the animal deviate from its original growth path. When favourable
conditions are restored, the animal often exhibits accelerated growth. In animal
production, most classical studies in compensatory growth have involved sheep
and cattle (ODonovan, 1984).
Two hypotheses have been put forward to explain the mechanisms that govern
compensatory growth. The first is the 'central control' hypothesis, which suggests
that the body has a set point for body size appropriate for a particular age and
that this control resides in the central nervous system (Wilson and Osbourn, 1960;
Mosier, 1986).After a period of undernutrition, the body tries to attain size that is
appropriate for age in the shortest possible time. The second is the 'peripheral
control' hypothesis, which suggests that control of body size is determined by the
tissues where cell number or, more accurately, DNA determines the extent of
growth following a period of undernutrition or illness (Winick and Noble, 1966;
Pitts, 1986).
Figure 1 is a schematic representation of different growth curves of broiler
chickens described by Leeson and Summers (1991). Lines A, B and C represent
three potential growth curves of broilers that reach approximately 2 kg body
weight at 42 days of age. If birds grow at a uniform rate, growth will be as
depicted by line B, and represents perhaps a biological ideal as far as minimizing
stress is concerned, i.e. continual steady growth with no major period of slow or
rapid growth. However, few animals grow with such 'statistical' precision. Birds
which grow through lines A and C both reach 2 kg weight at 42 days, yet the

190 World's Poultry Science Journal, Vol. 52, July 1996

 Compensatoy growth in the broiler chicken: A.K. Zubair and S . Leeson

Figure 1 Schematic representation of growth curves of broiler chickens. Reproduced from Leeson
and Summers (1991) with permission.

routes they take are quite dissimilar. Bird A has more rapid initial growth and,
subsequently, a slower growth approaching market weight. Bird C initially has a
slower rate of growth, followed by an accelerated growth towards market weight.
Bird C will probably exhibit a superior feed conversion because it will have a
lower maintenance requirement. The reason for this reduced maintenance
requirement is that, at any specific age, before reaching point X, the bird has a
smaller body mass to maintain and so will need less feed nutrients for this
purpose. Smaller birds have proportionately higher maintenance requirements,
but if C is sufficiently different from A there will be a reduction in the absolute
quantity of nutrients going towards maintenance. Totalling these reduced
maintenance needs, while still achieving the desired body weight (X, Figure Z),
must result in more feed directed to growth and so improved feed efficiency. This
theory assumes that carcass composition is unaltered.
Early studies of feed restriction programmes in broilers have been primarily
concerned with lowering body fat and improving feed efficiency (Griffiths et al.,
1977; Fisher, 1984) which, in many cases, were attained at the expense of final
body weight. Osbourn and Wilson (1960) and Auckland and Morris (1971)
demonstrated the feasibility of compensatory growth with chickens and turkeys
subjected to feed restriction during early life so that final body weight is not
compromised. Many studies since this time have reported the occurrence of
compensatory growth and the potentials for this to correct problems associated
with normal fast growth rate in the broiler chicken (Plavnik and Hurwitz, 1985;
1988a,b; 1991; Plavnik et al., 1986; Jones and Farrell, 1992a; Zubair and Leeson,
19944. These types of observation were repeatedly reported by Plavnik,
Hurwitz and co-workers in a series of studies with broilers and turkeys
(Plavnik et al., 1986; McMurtry et al., 1988; Plavnik and Hurwitz, 1988a,b; 1989;
1991). Other workers, however, failed to show complete growth compensation
under similar nutritional conditions (Yu et al., 1990; Jones and Farrell, 1992a;
Robinson et al., 1992; Zubair and Leeson, 1996). The variability in results of such

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Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
studies is due to a number of factors that influence the response of broiler
chickens to short-term early undernutrition.

Factors that influence compensatory growth in the broiler chicken

Factors that influence the ability of animals to exhibit compensatory growth
during the period of realimentation following nutritional deprivation were
identified by Osbourn and Wilson (1960). These factors include the nature,
severity and duration of undernutrition as well as the age at the commencement
of undernutrition and the degree and pattern of realimentation.

Duration and timing of undernutrition

Many studies have shown that the longer the period of undernutrition, the
more difficult it is for broilers to compensate for the reduction in weight gain (Yu
and Robinson, 1992).Feed restriction for a period of 6 days allowed for complete
body weight recovery, while recovery was not seen when restriction was more
prolonged at 12 days (Plavnik ef al., 1986). This situation is consistent with the
results of many other workers (Rosebrough et al., 1986; McMurtry ef al., 1988;
Ballay et al., 1992). Most workers recommend feed restriction of not more than 7
and 5 days for male and female broilers respectively, to allow for full body weight
recovery (McMurtry ef al., 1988; Plavnik and Hurwitz, 1991).Mollison et al. (1984)
restricted the feed intake of birds to 90% of that of control birds from 7 to 49 days
of age, and reported a significantly lower final body weight of 56 days of age. The
lack of recovery in body weight by the restricted birds was likely to have been
caused by the lengthy period of restriction, giving no time for the birds to exhibit
complete growth compensation. On the other hand, a feed restriction period of 4
days for female broilers allowed for full recovery in a much shorter time (Jones
and Farrell, 1992a). It is not clear whether milder restriction programmes of
shorter duration would have much effect on reducing body fat deposition, which
is one of the primary objectives of feed restriction.
Initiation of 6 days feed restriction at any age between 3 and 11days of age seems
to permit complete body weight recovery by 8 weeks of age in male broilers
(Plavnik and Hurwitz, 1988a). Similarly, other workers have recommended the
commencement of restriction at 5 to 7 days of age (Rosebrough et al., 1986).On the
other hand, Washburn and Bondari (1978) initiated their feed restriction
programme at 3 weeks of age, and reported very little evidence of compensatory
growth, probably because very little time was allowed for recovery.

Nature and severity of undernutrition

The level of restriction imposed is usually calculated to meet the maintenance
energy requirement of the birds, based on the recommendations of Plavnik and
Hurwitz (1989). These workers estimated the metabolizable energy (ME)
requirement for maintenance for male broilers to be 6.3 kJ/kg W0.67.More severe
restriction tends to compromise the ability of the bird to recover. The level of feed
restriction which Plavnik and Hurwitz (1989) estimated just to meet maintenance
energy requirements is equivalent to about 167 kJ ME/bird/day in the 6-12 day
period (approximately 35% of normal feed intake). This maintenance energy
level, however, must have been overestimated because the feed-restricted birds
gained 2-4g body weight each day during the restriction period. It is also
possible, as suggested by some workers, that the birds, even though in negative
energy balance, were able to gain weight due to change in body composition, i.e.

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 Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
used fat reserve and deposited more lean tissue (Leeson ef al., 1991; Yu and
Robinson, 1992). However, other workers were unable to demonstrate complete
compensatory growth of broilers which had been subjected to similar degrees of
feed restriction (Pinchasov ef al., 1985; Plavnik et al., 1986; Calvert ef al., 1987;
Pinchasov and Jensen, 1989; Yu et al., 1990; Robinson ef al., 1992). Later studies by
Plavnik and Hurwitz (1991) showed that milder restriction, which allowed
60-70% of normal growth, permits more realistic recovery. Similar methods of
feed restriction were successfully used by Pokniak and Cornejo (1982).
Leeson et al. (1991) used conventional broiler starter diets, which had been
diluted with 25%, 40% or 55% ground rice hulls, from 7 to 16 days of age, and
reported complete body weight recovery by all the treatment groups by 42 days
of age with no change in overall feed efficiency. This is particularly interesting
because the group that received the 55% diluted diet consumed 40% more feed
than control groups during the diet dilution period, presumably in an attempt
to meet energy needs for maintenance and growth. A similar study by Zubair
and Leeson (1994a) examined the effect of subdividing the 6 day period of
undernutrition on both growth performance and carcass characteristics of
broilers. It was calculated that male broilers would achieve an ME intake of
about 347 kJ per bird per day when given a diet which had been diluted with
50% oat hulls, which should meet their maintenance requirement and support
about 60% of their normal growth. Complete growth compensation was
achieved, with an improvement in overall efficiency of energy utilization.
Carcass characteristics, however, were not affected by early life undernutrition.
Subdividing the 6 day period of undernutrition did not alter growth perform-
ance or carcass characteristics at 42 and 49 days of age.
Jones and Farrell (1992a)restricted broilers to only 2.9 kJ/kg W0.67,a level much
more severe than that recommended by Plavnik and Hurwitz (1989), and
reported complete body weight recovery at 48 days of age. The restriction, which
was split into two periods of two days, rather than six or seven continuous days
as used more commonly by other workers, was applied for only four days. These
findings support the earlier suggestion by Wilson and Osboum (1960) that
compensatory growth after a period of undernutrition is greatest immediately
following realimentation. This led to the hypothesis that splitting the period of
feed restriction into shorter and less severe periods would cause the animals to
lose little or no weight, or even to gain some weight during the undernutrition
period, and so lead to fundamental difference in the response of birds to
realimentation (Jones and Farrell, 1992a). However, the results of Zubair and
Leeson (1994a) failed to support this concept.

Condition of realimentation
There is at present very limited information about energy and protein
requirements during the refeeding period. Plavnik and Hurwitz (1989) re-
evaluated the amino acid requirements of broilers during realimentation. Based
on the expected growth rate and body composition, their model calculations
showed higher requirements for most of the essential amino acids, especially
during the first 2 weeks of refeeding. A more recent study by Jones and Farrell
(1992a) demonstrated that dietary supplementation with lysine and/or methio-
nine during the refeeding period resulted in higher final body weight and leaner
carcasses. More consistent results of compensatory growth have been obtained in
studies that have extended the growth period to 8 weeks or more (Plavnik and
Hurwitz, 1985; 1988a; 19911; Plavnik ef al., 1986; Jones and Farrell, 1992a,b). It is

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Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
not clear whether growth compensation per se was achieved in some of these
studies due to an early plateau in the growth of control birds.

Genetic factors: effect of sex and strain of birds

Male broilers have a greater ability to exhibit compensatory growth following
a period of undernutrition than females (McMurty et al., 1988; Plavnik and
Hurwitz, 1991). This is probably because of differences in their innate growth
rates and body fat deposition (Fisher, 1984; Leenstra, 1986).The results of studies
by Plavnik and Hurwitz (1985; 1990) showed that males, but not females, were
able to exhibit complete compensatory growth when subjected to similar
conditions. The lack of consistency in the response of broilers to early
undernutrition programmes has been attributed by many workers to differences
in strains of birds used (Yu et al., 1990). Cherry et al. (1978) showed that fast
growing broiler strains exhibit little compensatory growth when compared with
slower growing strains.

Methods of nutrient restriction

Physical feed restriction
Various methods of undernutrition have been used by different workers to
retard or even stop growth during the undernutrition period. The most
commonly used method of feed restriction is simple physical restriction which
provides a calculated quantity of feed per bird, this often being just enough to
provide for maintenance energy requirement (6.3kJ/kg Wo.67/day;Plavnik and
Hurwitz, 1989).This method of feed restriction has the disadvantage of requiring
frequent weighing of feed. There is the additional problem of feeder space which,
if limiting, leads to non-uniform distribution of the small feed supply, thereby
causing uneven body weight distribution within a flock. Many workers have used
physical methods of feed restriction because birds can adapt to the feeding of high
fibre diets. Such adaptation enables them to digest, to some extent, the otherwise
indigestible fibre, thereby getting more energy (and possibly other nutrients) than
is required to achieve the desired growth retardation during the undernutrition
period. Leeson et al. (1991)reported more than expected growth for broilers fed a
diet containing 55% rice hulls, based on the calculated expected nutrient intake.
They suggested that the ingredients used for diet dilution, such as rice and oat
hulls, are assumed to contain little digestible energy, but may actually provide
substantial amounts of nutrients. Such a situation will obviously interfere with
the total energy intake of the birds during undernutrition, thereby changing the
growth pattern.

Diet dilution and chemical methods of feed restriction

While physical feed restriction is the most common technique used to achieve
undernutrition, in practical situations it is very difficult to distribute evenly feed
that provides only about 126-168 kJ ME/bird/day. With physical feed restriction
programmes there is also the problem of even distribution of micronutrients and
anticoccidial chemicals among the birds in a flock. An alternative system of
achieving uniform undernutrition within a flock is by diet dilution or the use of
other chemical means to restrict intake of specific nutrients or feed.
Leeson et al. (1991) replaced 25-55% of a conventional broiler starter diet with
rice hulls during a period of 7-14 days and showed complete recovery of body
weight by 42 days of age. In this study vitamin and mineral sources were not

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 Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
affected by the diet dilution. This is in agreement with results of Jones and Farrell
(1992a) who fed diets diluted up to 65% with rice hulls and also obtained
complete growth compensation relative to the control birds at 48 days of age. The
results of Leeson et al. (1991) showed no change in overall efficiency of feed
utilization, although the treatment birds utilized the diluted diet very efficiently
during the undernutrition period. Birds fed diluted diets eat more feed, which in
extreme situations can be up to 150% of normal intake (Leeson et al., 1991).
Restriction of feed intake of broilers by chemical means was suggested by
Fancher and Jensen (1988) as an alternative to diet dilution. These authors used
glycolic acid (GA) which is a naturally occurring compound in many foods and
has been reported to depress feed intake in a dose dependent manner in broiler
chicks. Pinchasov and Jensen (1989) used GA as a chemical means of restricting
feed intake of broilers, and compared this with the traditional physical feed
restriction method. During the restriction period (7-14 days) the feed intake of
birds given diets supplemented with 1.5% and 3.0% GA was depressed by 17%
and 45%, respectively. These reductions of feed intake due to GA supplementa-
tion resulted in growth retardation during the undernutrition period to 71% and
41 %, respectively, relative to the growth of control birds. Male broilers exhibited
complete body weight recovery at 49 days of age, with no difference between the
birds restricted by dietary GA addition or those subjected to physical feed
restriction. Due to its natural occurrence, GA may serve as a safe and useful
anorectic compound for restricting feed intake in poultry (Harris and Richardson,
1980). This method of feed restriction has the advantage of ensuring even
distribution of the feed and giving the birds appropriate intakes of micro-
ingredients such as anticoccidials.

Use of low protein or low energy diets

Achieving growth retardation by undernutrition may require extra labour or
mechanization to apply physical feed restriction, or the use of non-digestible
materials to dilute the feed. An alternative method of retarding early growth is the
restriction of intake of specific nutrients, such as protein (Moran, 1979). Broilers
require 220,200 and 180g/kg dietary crude protein during the starting, growing
and finishing periods, respectively, for optimal growth (NRC, 1994).They tend to
increase their feed intake to make up for deficiencies when fed diets that are
marginally deficient in crude protein (Fisher, 1984). However, feed intake is
depressed by feeding diets that are severely deficient in crude protein (Plavnik
and Hurwitz, 1990).
Studies by Plavnik and Hurwitz (1990) showed that ad libitum feeding of a diet
containing only 94 g/kg crude protein from 8 to 14 days decreased the feed intake
of broilers by some 57%. This decrease in feed intake resulted in 41% growth
retardation, which was not recovered after 6 weeks of realimentation. It is not
clear whether this inability for complete compensatory growth is related to the
birds previous protein intake.
Deaton et al. (1973) utilized a low energy diet to reduce body weight of broilers
by 4 weeks of age. By 8 weeks of age males fed a high energy diet were able to
compensate for the weight loss occurring during the preliminary feeding of low
energy diets. Females required less energy to recover from the lost body weight
than did males. Calvert et al. (1987) used two levels of diet ME (13.0 and 14.2MJ/
kg) during an undernutrition period of 6-12 days of age, and fed birds 167kJ ME
per bird per day. Complete growth compensation was observed by all growth-
retarded birds by 56 days of age.

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Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
Adipose development, fat deposition and compensatory growth in the
broiler chicken
Reports suggesting that fatness at an early age may affect adiposity at adulthood
led to the initiation of studies intended to elucidate whether nutrition at an early
age might have subsequent inductive effects (Nir et al., 1988).Nutritional studies
have indicated that the ages at which the different processes involved in adiposity
(hyperplasia and hypertrophy) occur can be altered by level of feeding, especially
at early ages (Pfaff and Austic, 1976). Feed restriction treatments are, therefore,
mostly imposed during the second to third week of age in broiler chickens, as an
attempt to alter hyperplastic growth of adipocytes which, at this age, accounts for
most of the growth of the adipose tissue. It is hypothesized that this will suppress
or delay adipocyte proliferation, and this is expected to be accompanied by lower
adiposity in older broilers.
The application of early undernutrition to reduce carcass fat content in the
broiler chickens has met with varying degrees of success. Reduction in body fat
and abdominal fat as a result of early feed restriction was achieved by a number
of workers (Plavnik and Hurwitz, 1985; 1990; 1991; Plavnik et al., 1986; McMurtry
et al., 1988;Jones and Farrell, 1992a,b),although a comparable number of studies
showed no real effect (Pokniak and Cornejo, 1982; Pokniak et al., 1984; Summers
et al., 1990; Yu et al., 1990; Zubair and Leeson, 1996). Beane et al. (1979) reported
that feed efficiency was improved, but that the size of the abdominal fat of male
broilers was significantly increased following feed restriction and refeeding. Very
interesting results of the effects of feed restriction in early life on body fat
deposition in broiler chickens were reported by Rosebrough et al. (1986) and
McMurtry et al. (1988). These authors reported depression in the activities of
enzymes associated with hepatic lipogenesis during undernutrition but, during
refeeding, there was a dramatic increase in such enzyme activities.After 2 weeks
of refeeding the activities of these enzymes (fatty acid synthetase, isocitrate
dehydrogenase and malic enzyme) declined to levels lower than those seen in ad
libitum fed control birds. The reason for such rebound, and then decline, in
lipogenic enzyme activities is not well understood. However, this inferred a lower
rate of lipid synthesis in the ’restricted-refed’broilers that may relate to the lower
carcass fat at 7 or 8 weeks reported by Plavnik and Hurwitz (1991) and Jones and
Farrell (1992a,b).
Results of a number of studies showed that, even though growth of adipose
tissue is controlled during feed restriction, adipose tissue is, however, capable of
hyperplasia during refeeding. Such adipocyte hyperplasia continues until the cell
number appropriate for the body mass is attained (Leclerq, 1984; Cartwright,
1991; Zubair and Leeson, 1996). A very strong positive relationship has been
reported between development of body mass and adipocyte hyperplasia in
broilers (Cartwright et al., 1988; Cartwright, 1991).These workers suggested that
adipose tissues from larger birds are hypoplastic relative to tissues from birds of
smaller body size. This hypothesis is not in agreement with that proposed by
some workers, that adiposity in chickens is influenced by nutritional conditions
during the early growth period (Pfaff and Austric, 1976; Nir et al., 1988). It may,
however, be possible that early feed restriction delays the recovery of cell number,
and this must be viewed in relation to the relatively short growth period of the
modern broiler chicken.
Severe feed restriction between 6 and 14 days, followed by ad libitum feeding,
resulted in less abdominal adipose tissue at 8 weeks of age (Plavnik and Hurwitz,

196 World’s Poultry Science Journal, Vol. 52, July 1996

 Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
1985; Jones and Farrell, 1992a,b).Restricting the feed intake of broiler chickens to
provide only 3.1kJ/kg Wo.67/dayduring the period 7-13 days of age resulted in
lower fat cell number and, as a consequence, decreased total body fat content,
with no adverse effect on final body weight at 56 days of age (Jones and Farrell,
1992b).These authors attributed the differences in the body fat contents between
the treatments to a delay in adipocyte hyperplasia, as a result of early feed
restriction. This hypothesis is consistent with the results of studies of porcine
adipose tissue conducted by Hood and Allen (1977),which showed that slowing
the rate of growth of an animal by feed restriction also delayed adipocyte
hyperplasia, but did not alter the total cell number at maturity.

Energy metabolism and compensatory growth in the broiler chicken

Many studies have reported that underfed animals exhibit metabolic adaptations
that include lower metabolic heat production (Forsum et al., 1981; Webb and
Abrams, 1983; Harris and Martin, 1984; Jones and Farrell, 1992a). It is
hypothesized that such adaptations continue into the refeeding period, and this
means improved feed efficiency. Other workers proposed that compensatory
growth relates to the reduction in maintenance requirements due to smaller body
size during refeeding (Wilson and Osbourn, 1960; Graham and Searle, 1975;
Dickerson, 1978).
Results of calorimetry studies by Zubair and Leeson (199413) demonstrated that
the lower metabolic rate in ’restricted-refed’broilers does not play a part in any
improved feed efficiency or growth compensation. Broilers undergoing 50% feed
restriction showed about 40% lower metabolic rate compared with their full-fed
counterparts (Figure 2). Calorimetric measurements taken after five days of
refeeding, however, indicated no difference in metabolic rate for the two groups
of birds (Zubair and Leeson, 1994b, Figure 2). Similar results were reported by
Jones and Farrell (199213) in broilers.

A B
12.5 12.5
12.0 12.0
11.5 11.5
11.0 11.0

10.5 10.5
P
0
10.0 p 10.0
3 9.5 3 9.5
f 9.0 p 9.0
8.5 8.5

8.0 8.0
7.5 7.5

7.0 7.0
6.5 6.5
0 12 24 36 0 12 24 36
Hours of fasting Hours of fasting

Figure 2 Metabolic rate of male broilers during 36 h feed removal starting on (A) day 11 and (8)day
18, either full-fed (-) or feed restricted (---) from 6 to 12 days of age. Data represent mean (SE) of three
replicates of 10 broilers each at each point. *“p<0.01. Reproduced from Zubair and Leeson (1994b)
with permission.

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Compensatory growth in the broiler chicken: A.K. Zubair and S . Leeson
A number of workers have proposed that energy and other nutrients which
support compensatory growth come from the reduction in maintenance require-
ment due to a smaller body size during refeeding (Wilson and Osbourn, 1960;
Graham and Searle, 1975; Dickerson, 1978). Restricted-refed broilers exhibit
higher feed intake relative to body weight compared with full-fed controls
(Zubair and Leeson, 1994b).This hypothesis supports the concept that the energy
required to support growth compensation during refeeding comes from a higher
feed intake relative to body weight. Another adaptation exhibited by the
restricted-refed broilers is the relative enlargement of digestive organs, especially
the crop, gizzard, pancreas and liver, which enhance feed intake and help support
compensatory growth (Zubair and Leeson, 1994b).

Conclusions
Over the past 10 years many studies have examined the effect on compensatory
growth, feed efficiency and body fat content of subjecting the broiler chicken to
early life undernutrition. Results of these studies have been very inconsistent, and
such discrepancies have been attributed to differences in factors such as method,
level and duration of undernutrition. Other factors that influence any compensa-
tory growth response are the nutritional conditions, duration of re-feeding and
bird strain. Dietary manipulations can be used to reduce body fatness by reducing
adipocyte hypertrophy and hyperplasia. Changes in cell size are, however, very
transitory, with the birds being able to attain normal adipocyte size within a few
days of refeeding. This makes success in lowering carcass fat in restricted-refed
broilers very difficult. A number of studies have reported lower carcass fat in
market age broilers, and this is attributed to a delay in adipocyte hyperplasia.
Improvements in feed efficiency, resulting from early feed restriction, have been
demonstrated in many studies. Lower metabolic rate per unit of body weight
does not seem to play a part in the ability of broilers to show improved feed
efficiency, and improved feed usage may simply relate to a greater feed intake
relative to body size in restricted-refed birds. Greater feed intake relative to body
weight, and its associated digestive adaptations, seem to be important contribut-
ing factors to any growth compensation. For more consistent results of
improvement in feed efficiencyand lower body fat content, there is need for more
studies to investigate the relationship between energy metabolism and develop-
ment of adipocytes at different ages. A good understanding of how these
processes are influenced by factors such as age, level, timing, and duration of
undernutrition is essential. Broiler nutrition during the period of expected growth
compensation has received little attention. Proper nutrition that will permit body
weight recovery and, at the same time, maintain a leaner body condition is
obviously advantageous. Such information would make the potential application
of short-term undernutrition in broiler production more realistic.

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