BREEDING AND GENETICS
Estimation of Growth Parameters Using a Nonlinear Mixed Gompertz Model
Z. Wang and M. J. Zuidhof1
Livestock Development Division, Alberta Agriculture, Food and Rural Development,
7000-113 St. Edmonton, Alberta, Canada, T6H 5T6
ABSTRACT In order to maximize the utility of simula-
tion models for decision making, accurate estimation of
growth parameters and associated variances is crucial. A
mixed Gompertz growth model was used to account for
between-bird variation and heterogeneous variance. The
mixed model had several advantages over the fixed ef-
fects model. The mixed model partitioned BW variation
into between- and within-bird variation, and the covari-
(Key words: broiler, nonlinear mixed model, Gompertz, growth parameter, inference)
INTRODUCTION
Comparisons of the characteristics of different broiler
strains can be used to identify and improve supply chain
efficiencies. In bioeconomic models, genotype-specific
growth curves are used to dynamically estimate daily
nutrient requirements at different ages (Hancock et al.,
1995; Gous, 1998; Gous et al., 1999, 2002). In order to
maximize the utility of simulation models for decision
making, accurate estimation of growth parameters and
related variances and covariances across age is crucial
(Hancock et al., 1995). Many broiler growth data analyses
(Emmans, 1995; Hancock et al., 1995; Gous et al., 1999)
have been conducted using the well-known Gompertz
(Gompertz, 1825; Emmans, 1981; Emmans and Fisher,
1986) growth function, which describes a single sigmoidal
growth phase. Typically, this growth curve is used to fit
longitudinal BW (Wt) data as a function of age (d) for a
particular genetic strain from age t = 0 to maturity. In
the current analysis of broiler chicken growth, maturity
was defined as the mature lean carcass, including bones,
muscles, and essential metabolic organs (Kwakkel et al.,
1993). More complex multiphasic models must be used
to account for other growth phases such as the develop-
ment of the reproductive tract, or the deposition of fat in
mature animals.
The Gompertz growth function is usually estimated
once per genotype (sex × strain), such that a common
2004 Poultry Science Association, Inc.
Received for publication September 19, 2003.
Accepted for publication December 29, 2003.
1
To whom correspondence should be addressed: martin.zuidhof@
gov.ab.ca.
847
ance structure assumed with the random effect accounted
for part of the BW correlation across ages in the same
individual. The amount of residual variance decreased
by over 55% with the mixed model. The mixed model
reduced estimation biases that resulted from selective
sampling. For analysis of longitudinal growth data, the
mixed effects growth model is recommended.
2004 Poultry Science 83:847–852
mature weight (Wm) is estimated for each genotype, and
a random error (eit) is associated with each individual
bird i at age t in the model, which is assumed to be an
independent normally distributed random variable with
mean of zero and a constant variance σe2. This model is
considered a fixed effect model because there is no ran-
dom effect associated with Wit. The results obtained with
fixed model analysis can sometimes be misleading, espe-
cially in the presence of competitive interaction and selec-
tive sampling (Le Dividich, 1999). Furthermore, repeated
measurements of BW from the same bird are likely to be
more closely correlated than measures made on different
birds, and measures made close in time on the same
individual are likely to be more highly correlated than
measures made further apart in time (Littell et al., 2000).
This type of underlying relationship, often inherent in
repeatedly measured growth data, contradicts the as-
sumption that eits are independent of each other with a
constant variance over ages. For this type of longitudinal
growth data, there are at least 2 sources of variation
(within and between individuals) in Wit. The fixed effect
model described above does not account for variability
between individuals (Craig and Schinckel, 2001), and it
also ignores the underlying relationships inherent in the
longitudinal growth data. The objectives of the current
study were 1) to account for at least a portion of increasing
BW variance as age increases, and greater serial correla-
tions at later ages; 2) to determine whether the mixed
model can reduce the effect of selective sampling and
competitive advantage on estimates of growth parame-
Abbreviation Key: BIC = Bayesian information criterion.
848 WANG AND ZUIDHOF
TABLE 1. Bayesian information criterion1 fit statistics for fixed and mixed Gompertz growth models
for females and males of 6 commercial boiler strains
Female
Strain Fixed model Mixed model
1 −427.1 −556.0
2 −364.5 −573.2
3 −278.9 −474.2
4 −215.0 −389.9
5 −316.3 −521.8
6 −216.3 −408.2
Average −303.0 −487.2
1
A lower value indicates a better fit of the model to the data.
ters; and 3) to compare the results with a corresponding
fixed effects Gompertz growth model.
MATERIALS AND METHODS
Experimental Design
The data for this analysis was taken from an experiment
with a 6 × 2 factorial arrangement of treatments, with 6
commercial broiler strain crosses (1 to 6) and 2 sexes (male
and female). Chicks were obtained from commercial
broiler breeder flocks. To minimize variation in initial
chick weight, parent flocks of similar age (46 ± 3 wk)
were used. At hatch, 960 chicks (80 chicks per strain-by-
sex combination) were individually identified and
weighed. A total of 120 chicks (10 per treatment) were
placed into each of 8 replicate pens and grown together
until 16 wk of age. Individual BW data were recorded
for each bird twice a week from 0 to 6 wk, weekly from
6 to 10 wk, and biweekly from 10 to 16 wk. Data were
recorded more often in the early part of the study because
the relative growth rate (as percentage of BW) was much
higher early, thus improving the rate of maturing esti-
mate. Because the trial from which these data were col-
lected involved serial dissections of individual birds
weekly to 6 wk, we used a subsample of 14 to 18 birds
per strain-by-sex combination having a complete set of
BW observations to 12 wk in the current analysis.
Because of a sexual maturity related growth spurt, data
after 12 wk were deleted from the data set. The sexual
maturity related growth spurt is a second phase of growth
(Kwakkel et al., 1993, 1995). Because the Gompertz func-
tion describes a single (prepubertal) growth phase, it was
legitimate and necessary to remove the bias of the sexual
maturity related growth spurt from the growth parameter
estimates of the first growth phase. This approach was
also taken by Hancock et al. (1995).
Bird Management and Nutrition
The care of the birds met the guidelines of the Canadian
Council of Animal Care (1993). Because the Gompertz
growth model describes nonlimited growth, care was
taken to ensure that the environment did not limit growth.
To provide a thermoneutral environment during brood-
Male
Fixed model Mixed model
−235.9 −396.7
−101.2 −334.3
−41.5 −218.3
−0.4 −181.7
−135.7 −328.1
−108.8 −352.7
−103.9 −302.0
ing, the facility was maintained at approximately 5°C
below the desired temperature at floor level in the central
hallway, and temperature gradients were established us-
ing thermostatically controlled gas brooders at the back
of each pen. Bird behavior and temperature data at bird
height in the center of each pen were monitored closely
to verify that birds in every pen had a broad thermoneu-
tral zone. To monitor environmental temperatures, tem-
perature data loggers were placed on a water line in
each pen and recorded the pen temperature at bird level
automatically every 15 min for the duration of the trial.
A photoschedule of 23L:1D was used throughout the trial
so that birds would have almost continual access to feed
and water. No vaccinations were provided, as the mount-
ing of an immune response would divert nutrients other-
wise channeled toward growth. Approximate stocking
density decreased from 10 birds per m2 at hatch to 4 birds
per m2 by 6 wk.
Starter (0 to 21 d), grower (21 to 35 d), roaster (35 to
49 d), and roaster II (49 to 112 d) diets were formulated
to provide 100 and 105% of NRC (1994) recommended
energy and protein levels (formulated on the first 3 amino
acids that were most likely to be limiting: lysine, total
sulfur amino acids, and threonine), respectively. Ade-
quate feeder space (5 cm per bird) and water nipple avail-
ability (15 birds per water nipple) was provided to ensure
that these factors would not limit rates of gain. Ad libitum
access to feed and water was provided for the duration
of the trial.
Broiler Growth Model
The broiler growth data was fitted to the fixed effect
Gompertz growth function proposed by Emmans (1981).
Wit = Wmexp(−exp(b(t−t*))) + eit, [1]
and the mean and variance can be expressed as
E(Wit) = Wmexp(−exp(b(t−t*))) [2]
V(Wit) = V(eit) = σe2
where Wit is the expected BW of individual i at age t
days; Wm is the average mature BW of all birds in the
same group; b is a rate of maturing; t* is the time in days
 NONLINEAR MIXED GROWTH MODEL 849
TABLE 2. Growth parameters and standard error estimates of females and males of 6 commercial boiler strains determined
by fixed1 and mixed2 effect Gompertz growth models

Female Male

Fixed model Mixed model Fixed model Mixed model

3
Strain Parameter Estimate SE df Estimate SE df Estimate SE df Estimate SE df

1 Wm 4.776 0.043 283 4.753 0.055 16 6.141 0.070 282 6.057 0.083 16
b 0.0416 0.0003 283 0.0415 0.0002 16 0.0396 0.0003 282 0.0398 0.0003 16
σe2 0.0122 0.0010 283 0.0067 0.0006 16 0.0239 0.0020 282 0.0116 0.0010 16
σu2 0.0364 0.0141 16 0.0983 0.0359 16
2 Wm 5.003 0.049 300 4.962 0.063 17 6.514 0.090 302 6.498 0.108 17
b 0.0411 0.0003 300 0.0410 0.0002 17 0.0383 0.0004 302 0.0382 0.0003 17
σe2 0.0164 0.0013 300 0.0069 0.0006 17 0.0396 0.0032 302 0.0153 0.0013 17
σu2 0.0624 0.0223 17 0.1973 0.0687 17
3 Wm 4.955 0.057 300 4.885 0.079 17 6.152 0.093 283 6.159 0.114 16
b 0.0416 0.0004 300 0.0414 0.0003 17 0.0405 0.0005 283 0.0403 0.0003 16
σe2 0.0218 0.0018 300 0.0096 0.0008 17 0.0476 0.0040 283 0.0218 0.0019 16
σu2 0.0859 0.0329 17 0.1841 0.0671 16
4 Wm 4.792 0.061 300 4.664 0.087 17 6.611 0.121 233 6.653 0.144 13
b 0.0422 0.0004 300 0.0421 0.0003 17 0.0386 0.0005 233 0.0383 0.0004 13
σe2 0.0270 0.0022 300 0.0128 0.0011 17 0.0545 0.0050 233 0.0212 0.0020 13
σu2 0.1016 0.0399 17 0.2655 0.1048 13
5 Wm 5.069 0.058 249 5.094 0.070 14 7.076 0.122 249 7.123 0.122 14
b 0.0397 0.0003 249 0.0395 0.0002 14 0.0357 0.0004 249 0.0356 0.0003 14
σe2 0.0154 0.0014 249 0.0057 0.0005 14 0.0318 0.0028 249 0.0124 0.0011 14
σu2 0.0694 0.0265 14 0.2007 0.0764 14
6 Wm 5.504 0.069 234 5.439 0.089 13 7.187 0.102 251 7.205 0.118 14
b 0.0400 0.0004 234 0.0400 0.0003 13 0.0372 0.0004 251 0.0372 0.0002 14
σe2 0.0217 0.0020 234 0.0080 0.0008 13 0.0355 0.0032 251 0.0111 0.0010 14
σu2 0.1001 0.0408 13 0.2128 0.0799 14
1
Wit = Wmexp(−exp(b(t−t*))) + eit.
2
Wit = (Wm + ui)exp(−exp(b(t−t*))) + eit.
Wm = mature body weight (kg); b = rate of maturing (d−1); σe2 = the residual BW variance (kg); σu2 = the individual variance in Wm within a
3

population (kg).

at which growth rate is maximum, which can be obtained E(Wit) = ƒ(t; θ)

as t* = ln(−ln(W0/Wm))/b if the initial chick weight (W0)
is known; and eit is the residual BW of individual i at age
t. The eits are assumed to be normally distributed with
mean 0 and a constant variance σe2. The same data set was
also fitted to the mixed effect Gompertz growth function
Wit = (Wm + ui)exp−exp(b(t−t*))) + eit
where ui is a random deviation of mature BW of the
individual i from the average mature BW of its genotype
Wm. The uis are assumed to be normally distributed with
mean 0 and variance σu2 and independent of eit. The rest
of the terms are the same as in equation [1].
To fit the ui in the model is to allow the mature BW
Wim of each bird to vary among birds (Wim = Wm + ui) in
each sex and strain group. This mixed effect growth
model can also be written as
Wit = ƒ(t; θ) + uig(t; θ) + eit
where θ = {Wm, b}, such that the random effect ui is
multiplied by g(t; θ) = exp(−exp(b(t−t*))). The mean, variance
and covariance of the mixed effect growth model [4] can
be expressed as
V(Wit) = σu2g2 (t; θ) + σe2 [5]
Cov(Wit,Wit + j) = σu2g(t; θ)g(t + j; θ)
Because the mean of the random effect ui is 0 for a popula-
tion, the birds in each genotype follow the function ƒ;
this is the same as in the fixed effect model [1]. However,
[3] the advantages of the mixed model over the fixed model
are the ability to separate between- and within-bird varia-
tion, the ability to account for a portion of the increasing
variance in BW as age increases, and greater serial correla-
tions at later ages resulting from greater BW variation.
Because the function g increases with t, the covariance
structure increases with t such that Cov(Wit, Wit + 1) <
Cov(Wit, Wit + 2). This pattern of the variance and covari-
ance structures usually occurs in repeatedly measured
growth data (Craig and Schinckel, 2001).
Culling and Selection
[4] The mixed effects model handles selective sampling
problems in animal growth experiments better than a
fixed effects model (Craig and Schinckel, 2001). In broiler
growth trials, birds that fail to thrive due to sickness or
other reasons may be culled before the experiment is
completed. The earlier removal (involuntary culling) of
850 WANG AND ZUIDHOF
TABLE 3. Comparison of mature weight (Wm) parameter estimate using complete data set, and after
selective culling. Estimates were derived using fixed and mixed effect Gompertz growth models

Female Male

Fixed model Mixed model Fixed model Mixed model

1 2 3 1 2 3 1 2 3 1
Strain Cull All Bias Cull All Bias Cull All Bias Cull All2 Bias3

1 4.951 4.776 3.7 4.809 4.753 1.2 6.372 6.141 3.8 6.177 6.057 2.0
2 5.243 5.003 4.8 5.046 4.962 1.7 7.013 6.514 7.7 6.658 6.498 2.5
3 5.182 4.955 4.6 4.957 4.885 1.5 6.835 6.152 11.1 6.479 6.159 5.2
4 4.983 4.792 4.0 4.719 4.664 1.2 7.222 6.611 9.2 6.923 6.653 4.1
5 5.398 5.069 6.5 5.155 5.094 1.2 7.635 7.076 7.9 7.330 7.123 2.9
6 5.827 5.504 5.9 5.530 5.439 1.7 7.588 7.187 5.6 7.432 7.205 3.1
1
Estimates obtained with selectively culled data.
2
Estimates obtained with the complete data set.
3
Bias of estimate expressed as a percentage of inflation of the parameter estimates with selectively culled
data: bias = (Cull1–All2)/All2) × 100.

these slow growers from the trials may result in bias of
the growth parameter estimates. In order to show the
ability of the mixed model to handle this selective culling
problem, the bottom 8% of the slower growing birds at
age 70 d were removed from each strain and sex and
the remainder of the data were fitted to the fixed and
mixed models.
Statistical Analysis
A total of 3,266 longitudinal BW observations from 96
males and 100 females of 6 commercial broiler strains
were used in this analysis. The same data set was fitted
to the fixed [1] and mixed [3] effects growth models using
the NLMIXED procedure in SAS software (SAS Institute,
1999) to compare the results obtained from both models.
The Bayesian information criteria (BIC) fit statistic pro-
vided by NLMIXED procedure for both models was used
to evaluate the appropriateness of the 2 models. The BIC
values do not have an upper or lower limit, and do not
imply significant differences between models. However,
a lower BIC value indicates a better fit of the model to
the data. Parameters estimated by the model with lower
BIC scores increase the probability of obtaining the ob-
served data.
RESULTS AND DISCUSSION
Fit Statistics
The BIC fit statistics for fixed and mixed models are
summarized in Table 1 for each strain and sex. The BIC
values of the mixed models were all substantially lower
than those from the corresponding fixed model. The aver-
age BIC value over the 6 strains for the mixed model was
reduced 184.2 (−487.2 vs. −303.0) for female birds and
198.1 (−302.0 vs −103.9) for male birds. Overall, these fit
statistics indicated that mixed models fit the data better
than those of the fixed models.
Parameter Estimates
Estimates of the growth parameters obtained with the
fixed and mixed effects models are summarized in Table
2. For specific genotypes, the estimates of Wm and b from
fixed and mixed growth models were similar because the
expected means for both models are the same. The SE of
the Wm estimates obtained from the mixed model were
higher than corresponding SE estimates from the fixed
model but lower for the b and σe2 estimates. With the
mixed model, the average increase in Wm SE over the 6
strains was 31% for females and 15% for males. This

TABLE 4. The estimated residual variance,1 covariance,2 and correlation3 across age from d 7 to 49
with fixed growth model for strain 2 of female broilers

Age (d) 7 14 21 28 35 42 49
7 0.00028 0.00050 0.00058 0.00067 0.00054 0.00062 0.00024
14 0.80799 0.00138 0.00139 0.00179 0.00155 0.00156 0.00044
21 0.72330 0.77593 0.00234 0.00300 0.00263 0.00194 0.00098
28 0.56945 0.68105 0.87733 0.00498 0.00450 0.00417 0.00362
35 0.41576 0.53657 0.70003 0.82181 0.00602 0.00506 0.00422
42 0.42539 0.48381 0.46324 0.68238 0.75367 0.00750 0.00766
49 0.12048 0.09785 0.16956 0.42781 0.45402 0.73694 0.01438
1
The variances are on the upper left to lower right diagonal of the table.
2
The covariances are in the upper right triangle of the table.
3
The correlations are in the lower left triangle of the table.
 NONLINEAR MIXED GROWTH MODEL
increase was likely due to the very large decrease in the
number of degrees of freedom with the mixed model
(Table 2). With the mixed model, the average reduction
in SE for b was 29% for females and 28% for males. Most
importantly, due to variance partitioning, residual vari-
ances (σe2) obtained from the mixed model were reduced
55% in females and 59% in males in the mixed model
compared with the fixed model. This result represents
an improvement in estimation accuracy using the mixed
model. The variance estimates for the random effect u
were all significant (P < 0.05), indicating that the mixed
model accounted for between-bird variation in mature
BW. Fitting this random effect in the model allows Wit
to vary from the genotype mean, which is appropriate,
because mature BW of individuals are not identical. From
a growth modeling perspective, more accurate parameter
estimation will lead to better simulation to predict per-
formance.
The BIC and variance estimates inferred that the mixed
model was a better way to estimate growth parameters.
The additional random effect u allowed partitioning of
the Wt variation into between- and within-bird variation
and allowed the Wim of individual birds to vary around
the genotype mean. More importantly, the variance and
covariance structure [5] associated with the random effect
u in the mixed model can account for a good portion of
the increasing Wt variance as age increases. This finding
explained at least a portion of the age-associated increases
in variance and correlations across ages that were com-
mon in longitudinal growth data.
Culling and Selection
The results of the selective culling are summarized in
Table 3. Selective culling mainly caused the Wm parameter
estimates to inflate upward. The inflation was very small
with the estimates of parameter b and could therefore be
ignored. The magnitude of the inflation of the Wm esti-
mate with the fixed model (3.7 to 6.5% for females and
3.8 to 11.1% for males) was much larger than that esti-
mated with the mixed model (1.2 to 1.7% for females and
2.0 to 5.1% for males). The smaller bias resulted from
the variance and covariance structure associated with the
random factor u in the mixed model, which allowed the
mixed model to use information in the variance covari-
ance matrix, u, and information from those birds prior to
culling. Therefore, with the mixed model, estimation bias
resulting from selective culling was reduced compared
with the fixed model. This result was consistent with the
work of Craig and Schinckel (2001).
Violation of Residual
Variance Assumptions
As mentioned earlier, growth data often show an inher-
ent underlying relationship. Measures made on the same
individual are likely to be more closely correlated than
measures made on different individuals, and measures
made close in time on the same individual are likely to
851
be more highly correlated than measures made further
apart in time. Although the present experiment was de-
signed to allow all birds to express their genetic potential
for growth, these types of relationships may still exist. A
summary of residual variances, covariances, and correla-
tions across age for the females of strain 2 is presented
in Table 4 to illustrate the violation of fixed model as-
sumptions about the distribution of residuals. It is clear
that the variances along the diagonal increased with age,
and the covariances among the adjacent sequential resid-
uals also increased as age increased. The pattern was
similar to the variance and covariance structures assumed
for the random effects in the mixed model [5]. The addi-
tion of the random effect in the mixed model accounted
for a part of these heterogeneous variances and covari-
ance effects in the data, although not all. The net result
was improved precision in the estimation of growth pa-
rameters and a decrease in residual variance, ultimately
resulting in more accurate inferences based on these esti-
mates. As modeling becomes a more important tool for
predicting growth and performance, it is paramount that
those reporting growth parameters report not only geno-
type means and standard errors, but also an estimate of
the variation between birds within genotypes.
As with the fixed model, residual errors from the mixed
growth model were assumed to be randomly indepen-
dent normally distributed with mean of zero and variance
of σe2. However, for the growth data in the current study,
this assumption was not valid. Although the addition of
the random factor ui into the model removed heteroge-
neous variance and correlation across age, it did not re-
move all of this variation. Further theoretical studies are
encouraged to develop a mixed model with more appro-
priate covariance structures for residuals.
ACKNOWLEDGMENTS
The financial assistance of the Alberta Agricultural Re-
search Institute and the Alberta Chicken Producers. In-
kind assistance of Lilydale Poultry Company is gratefully
acknowledged. Thanks to David Eisenbart for excellent
technical assistance.
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