TSP & Calf Health: Holstein Dairy Calf Growth Performance

DOI: 10.1002/vms3.1203
ORIGINAL ARTICLE
24-Hour postnatal total serum protein concentration affects
the health and growth performance of female Holstein
dairy calves
Mitra Aghakhani1
Majid Toghyani1
Amir Davar Foroozandeh Shahraki1
Seyed Nouroldin Tabatabaei1
Erfaneh Moosavi-Zadeh1
Hassan Rafiee2
1
Department of Animal Science, Isfahan
(Khorasgan) Branch, Islamic Azad University,
Isfahan, Iran
Abstract
Background: Total serum protein (TSP) within the first few days of life in the neonatal
2
Animal Science Research Department,
Isfahan Agriculture and Natural resources
Research and Education Center, Agriculture
Research, Education and Extension
Organization (AREEO), Isfahan, Iran
calf has predictive value for subsequent growth and production in calves before and
after weaning.
Introduction: The objective of this study was to evaluate the effect of TSP concentration 24-h after birth (24-h) on the performance and health of Holstein dairy
Correspondence
Hassan Rafiee, Animal Science Research
Department, Isfahan Agriculture and Natural
resources Research and Education Center;
Agriculture Research, Education and
Extension Organization (AREEO),
8174835117 Isfahan, Iran.
Email: [email protected]
calves.
Methods: A total of 152 female calves were enrolled in this study. Blood samples
were collected at 24-h, and TSP concentration was measured with a refractometer.
Calves based on TSP concentration at 24-h were allocated into three groups: 1 – TSP
≤6.5 g/dL, 2 – TSP between 6.6 and 6.9 g/dL and 3 – TSP ≥7 g/dL. The weighing was
done at birth and at days 30 and 60. Starter feed intake was recorded from day 3 to
weaning, and body structures were measured at birth and weaning day.
Results: Calves with TSP >6.5 g/dL had greater body weight at days 30 and 60 than
calves with TSP ≤6.5 g/dL. Average daily gain during 1–30 and 1–60 days of life
increased as TSP increased. Furthermore, starter feed intake during the first 60 days of
life was greater in calves with TSP ≥7 g/dL than calves with TSP <7 g/dL. The TSP concentration influenced structural growth, and >6.5 g/dL calves had greater heart girth,
hip width and body length than ≤6.5 g/dL calves. Moreover, odds ratio for pneumonia
decreased as TSP increased, whereas diarrhoea was unaffected.
Conclusion: The TSP at 24-h is an important contributing factor for the variation in
growth performance and health of preweaning calves, and strategies to improve calf
immunity and increase TSP lead to better animal health during preweaning period.
Implications: These results indicated that TSP ≥6.5 g/dL possibly was associated with
greater performance, and this concentration could be considered a baseline for future
analyses.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided
the original work is properly cited.
© 2023 The Authors. Veterinary Medicine and Science published by John Wiley & Sons Ltd.
2230
wileyonlinelibrary.com/journal/vms3
Vet Med Sci. 2023;9:2230–2237.
KEYWORDS
body structures, dairy calves, growth, health, total serum protein
1
INTRODUCTION
tration after birth with body weight (BW) and average daily gain
(ADG) during the first 21 (Elsohaby et al., 2019) and 180 (Robi-
Bovine colostrum is defined as first secretion after parturition and
son et al., 1988) days of life in dairy calves. Robison et al. (1988)
contains higher protein, immunoglobulins, non-protein nitrogen, fat,
reported that mortality of heifer calves through 6 months of age with
vitamins and minerals compared to normal milk (Kelly, 2003). Due to
FPT was 6.78% compared with 3.33% mortality for calves with ade-
the absence of transfer of antibodies by placental blood to the calf dur-
quate passive immunity. In addition, calves that survived with FPT
ing gestation, the transfer of passive immunity through the absorption
failed to grow rapidly through 180 days of age. Furthermore, calf
of antibodies from colostrum is essential for neonatal calves. There-
serum Ig concentration 24–48 h after birth was a significant source
fore, colostrum management and providing high-quality colostrum in
of variation in mature milk and fat production, and heifers with FPT
proper time and volume are well recognized as vital in preventing
had lower milk production during their first lactation (Denise et al.,
disease during a period that the immune system will gradually acti-
1989).
vate in neonatal calves (Godden et al., 2019). Colostrum quality is well
In the previous studies, the suggested cut-off values for the FPT
defined by immunoglobulin G (IgG) concentration less than 2.0 g/dL as
using a refractometer were <5.2 g/dL TSP in healthy calves (Tyler
poor quality, 2.0–5.0 g/dL as moderate quality and finally the greater
et al., 1996; Windeyer et al., 2014) and <5.5 g/dL TSP in clinically
than 5.0 g/dL as excellent quality (Shearer et al., 1992). The current
ill calves (McGuirk & Collins, 2004; Tyler et al., 1996). Furthermore,
recommendation is the intake of colostrum containing the IgG concen-
Donovan et al. (1998), in a large study with 3300 female calves, indi-
tration >5.0 g/dL during the first 6–8 h of life. It is well demonstrated
cated the lowest risk of calves’ mortality and morbidity until 6 months
that colostral IgG concentration will peak approximately 24–36 h after
of life was associated with TSP >6.5 g/dL, and suggested this level will
feeding colostrum (Hassig et al., 2007). Therefore, if the serum IgG con-
be considered the baseline for future analyses. Moreover, Manriquez
centration exceeded 1.0 g/dL during that time, calves to be relatively
et al. (2018) categorized concentrations of TSP as low (≤6.5 g/dL);
well protected against pathogens (McGuirk & Collins, 2004). In a recent
medium (6.6–7.4 g/dL); or high (≥7.5 g/dL). Furthermore, Lombard et al.
study, four serum IgG categories were proposed including excellent,
(2020) reported in a systematic review that calves with TSP ≥6.2 g/dL
good, fair and poor with serum IgG levels of ≥2.5, 1.8–2.49, 1.0–1.79
have an excellent transfer of passive immunity. Based on these studies
and <1.0 g/dL, respectively (Lombard et al., 2020). These researchers
(Donovan et al., 1998; Lombard et al., 2020; Manriquez et al., 2018),
showed a reduction in morbidity and mortality rates with increasing
it seems that calves with TSP >6.5 g/dL have an excellent transfer of
serum IgG levels.
passive immunity and lowest risk of mortality and morbidity until 6
Total serum protein (TSP) or IgG concentration within the first few
months of life and suggesting that TSP >6.5 g/dL will be considered
days of life is the primary indexes for the failure of passive trans-
the baseline for future analyses. We categorized concentrations of TSP
fer (FPT) (Godden et al., 2019). In the neonatal calf, IgG constitutes a
as low (≤6.5 g/dL); medium (6.6–6.9 g/dL); or high (≥7.0 g/dL) for eval-
large proportion of the protein in serum. This allows the measurement
uating the TSP concentration on calves’ performance in the current
of TSP to provide an estimation of serum IgG concentration (Morrill
experiment.
& Tyler, 2012). The TSP measurement is more practical in farm con-
However, to our knowledge, there is limited information about the
ditions, as well as highly correlated with blood IgG concentration in
association between TSP concentration at 24-h and BW, ADG, starter
calves (Thornhill et al., 2015). Many articles used refractometers for
feed intake, body structure growth and morbidity in the preweaning
measuring the TSP (Cuttance et al., 2019; Hue, Williams, et al., 2021;
period for dairy calves. Therefore, this study aimed to assess the effects
Hue, Skirving, et al., 2021; Vogels et al., 2013). Hue, Williams et al.
of calves’ TSP concentration during the first 24 h after colostrum feed-
(2021) reported that serum protein refractometer measurements pre-
ing on health, growth performance and starter feed intake of female
dicted serum IgG level with high accuracy, providing an on-farm test
Holstein dairy calves.
to determine that calves have received sufficient passive immunity and
colostrum components.
Moreover, passive transfer of immunity has predictive value for
2
MATERIALS AND METHODS
subsequent growth and production in calves before and after weaning (Denise et al., 1989; Elsohaby et al., 2019; Robinson et al., 1998).
The FPT was associated with underdevelopment of the digestive
2.1
Experimental design, cow management and
treatments
tract and lower feed intake, resulting in reduced growth rates during rearing, and decreased milk production during the first lactation,
The experiment was carried out in a large commercial dairy herd, con-
compared with calves that had adequate passive immunity (DeNise
sisting of 3500 lactating cows in the Isfahan district during autumn
et al., 1989; Donovan et al., 1998; Robison et al., 1988). For example,
2018 with mean temperature and relative humidity 7◦ C and 51%,
a significant association was indicated between serum IgG concen-
respectively.
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2231
AGHAKHANI ET AL.
AGHAKHANI ET AL.
For this experiment, a total of 152 female Holstein dairy calves
Calves were monitored individually twice daily (before milk feed-
(39.0 ± 4.7 kg of initial BW), without birth defects, having been deliv-
ing) for any signs of ill thrifty, such as weakness, decreased appetite,
ered without assistance, and showing a regular respiratory pattern,
dehydration, fever, abnormal faecal consistency, increased respiratory
were eligible for enrolment. It was suggested in the literature that TSP
rate and other lethargy signs. Faeces were scored daily according to
≥6.5 g/dL would be considered the baseline for future analyses, and the
the procedure of Habibi et al. (2020) and categorized as firm and well-
calves based on TSP concentration at 24 h of life (24-h) were allocated
formed (score 1), soft and pudding-like (score 2), runny and pancake
into three experimental groups: 1 – TSP concentration ≤6.5 g/dL, 2 –
batter (score 3) and liquid and splatters (score 4). A diarrheic calf was
TSP concentration between 6.6 and 6.9 g/dL and 3 – TSP concentration
considered if the faecal score was ≥3. If having a faecal score ≥3 and
≥7 g/dL.
coughing or nasal discharge, the calves were examined by the veteri-
The calves were separated within 10 min after birth, not allowed
narian to confirm diarrhoea or pneumonia (Habibi et al., 2020). The
to suckle on their dams, weighed and moved to individual pens
treatment procedures for diarrhoea and pneumonia were applied at
(1.22 × 2.44 m) with sawdust bedding. Calves were weighed on an elec-
the FKA Milk and Meat Co. (Isfahan). Treatments were discontinued in
tronic scale and fed maternal colostrum based on an average of 10%
calves that did not respond to the treatment. No animal died during the
of their birth weight, approximately 30 min after separation from their
study.
dam. If all colostrum was not consumed, the remainder was fed 2 h later
after birth. According to farm protocol, the colostrum was harvested
within 30 min postpartum using a portable milking machine. Colostrum
of individual cows was milked into clean buckets and fed to their calves
in bottles according to their BW. Colostrum feeding was followed by
feeding 3 L of transitional milk per day until day 3. The transitional milk
from all dams was pooled and all calves fed transitional milk with similar quality. In the current experiment, transition milk is the milk that
cows produce after colostrum during second and third milkings. After
that, calves received whole milk (mean composition: 3.6% ± 0.13% fat,
3.2% ± 0.01% CP, 4.8% ± 0.15% lactose and 12.8% ± 0.52% total solids)
in galvanized buckets twice daily at 0800 and 1500 h until weaning. All
calves were fed 5 L/day of milk from day 4 to 15 and offered 6 L/day
of milk from day 16 to 21 of age and then 7 L/day from day 22 to 50
and 4 L/day from day 51–56 and 2 L/day from day 57–60 (total milk
offered = 331 L).
At day 4, calves were fed starter feed containing 224 g/kg CP,
2.3
Blood sampling and measurements
Blood samples were taken approximately at 24-h after birth from the
jugular vein into untreated evacuated tubes. The blood samples were
centrifuged at 1500 × g for 15 min at 4◦ C, and the serum was analysed using an optical protein refractometer (Instrument-Model PA203;
US patent D510880) for total protein. TSP was measured twice using
a refractometer, and the mean of these measurements was recorded.
Distilled water was used to calibrate the refractometer before each
use.
Colostrum samples were collected in 50 mL in plain evacuated
serum tubes (BD Vacutainer, Becton, Dickinson and Co., Belliver Industrial Estate) per cow for IgG analyses by ELISA sandwich method
(Bovine IgG ELISA Bioassay Tech. Lab E0010Bo Kit, assay sensitivity of
1.03 μg/mL and Intra and inter-CV were <8.00% and <10.00%).
39 g/kg ether extract and 11.79 MJ/kg ME on a DM basis prepared
as a mashed form. Starter feed was formulated according to CNCPS
2.4
Experimental design and analysis
and calves had free access to starter feed by offering an amount that
resulted in the residue of 10% of offered feed after 24 h. Through the
At first, a linear regression was used to assess the linear relationship
experiment, calves had free access to the starter feed and fresh water
between TSP concentration at 24-h with performance traits (BW at day
from the nipple.
60 and ADG).
To evaluate the effect of TSP on calf performance factors (growth
traits and starter feed intake) linear mixed model (PROC MIXED) was
2.2
Sampling and measurements
used. For traits such as starter feed intake with repetitions during the
experiment, they were analysed as repeated measurement. Also, to
BW was measured at birth, days 30 and 60 of life about 4 h after morn-
estimate the odds ratio of disorders due to differences in TSP at 24-
ing milk feeding. Starter refusals were recorded and renewed every
h used a logistic regression model with PROC GLIMMIX assumed a
day at 10:00 AM. The starter feed intake of each calf was calculated
binary distribution with the logit link function. All statistical analysis
from the difference between the daily starter feed that was offered and
was conducted using the SAS/STAT 9.4 (SAS Institute Inc.). Addition-
refused. Means of ADG were determined.
ally, the differences among the treatments were evaluated using a
Body measurements of each calf include body length (distance
multiple comparison test following the Tukey–Kramer method. Sta-
between the points of shoulder and rump), withers height (distance
tistical significance of any main effect was declared at p ≤ 0.05. The
from the base of the front feet to the withers), body barrel (circum-
statistical model used for the analyses was as follows:
ference of the belly before feeding), heart girth (circumference of the
chest), hip height (distance from the base of the rear feet to hook bones)
and hip-width (distance between the points of hook bones) were mea-
Yijklm = μ + TPi + Periodj + β1 × Bweightk + β2 × Bstral + Calfm
+ TPi × Periodj + eijklm
sured with calipers at the birth and weaning (day 60) according to the
where Yijklm is the dependent variable (weight as continuous; disor-
method described by Mirzakhani et al. (2021).
ders as binomial trait; starter feed intake as continuous; and structure
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2232
TA B L E 1
Descriptive statistics for 152 Holstein calves enrolled in the current study.
Items
Mean (± SD)
Minimum
Total serum protein at 24 h (g/dL)
6.7 ± 0.6
5.3
Maximum
8.9
Colostrum’s IgG (mg/mL)
84.1 ± 15.0
45.2
116.5
Birth weight (kg)
39.0 ± 4.7
25.0
50.0
Body weight at day 30 (kg)
48.3 ± 7.4
33.0
69.0
Body weight at day 60 (kg)
70.9 ± 10.1
41.0
91.0
TA B L E 2 Results of the final linear relationship for serum total
protein and calves’ growth performance.
Variables
Estimate (± SE)
p Value
Body weight at 60 day (kg)
Intercept
27.00 ± 7.80
0.007
Total serum protein
6.53 ± 1.15
<0.001
Intercept
603.61 ± 162.25
0.003
Total serum protein
23.04 ± 14.61
0.04
Average daily gain (g/day)
F I G U R E 1 Distribution of total serum protein concentration
(g/dL) at 24 h of life of 152 female Holstein calves.
growth traits as continuous); TPi is the TSP at 24-h (three levels; 1:
≤6.5 g/dL; 2: between 6.5 and 6.9 g/dL; and 3: ≥7.0 g/dL) as an independent variable, periodj is the measurement time, β1 and β2 are
regression coefficient for birth weight and birth structure traits (e.g.
heart girth and withers height) and Bweightk and Bstral are covariates
of birth weight and birth structure, respectively, TPi × periodj is the
interaction of TSP and measurement time, Calfm is the random effect
of calf and eijkl is the random residual error.
3
RESULTS
F I G U R E 2 Starter feed intake during the first 8 weeks of life with
three levels of total serum protein (TSP) at 24 h of life.
Results of descriptive analysis for TSP concentration at 24-h,
life increased as TSP increased, whereas ADG was greater during 30–
colostrum’s IgG concentration, birth weight and BW at days 30
60 days of life in calves with TSP ≥7 g/dL than calves with TSP <7 g/dL.
and 60 of Holstein dairy calves are presented in Table 1. TSP con-
Moreover, starter feed intake during the first 60 day of life was greater
centration at 24-h ranged from 5.3 to 8.9 g/dL, colostrum’s IgG
in calves with TSP ≥7 g/dL than calves with TSP <7 g/dL, and there
concentration ranged from 45.2 to 116.5 mg/mL, birth weight ranged
was no significant difference between calves with TSP ≤6.5 g/dL and
from 25 to 50 kg, BW at day 30 ranged from 33 to 69 kg and BW
between 6.6 and 6.9 g/dL (Figure 2).
at day 60 ranged from 41 to 91 kg. Furthermore, the distribution of
The results of structural growth are listed in Table 4. The TSP at 24-
TSP concentration at 24-h of 152 calves used in the current study is
h influenced structural growth, and >6.5 g/dL calves had greater heart
presented in Figure 1.
girth, hip width and body length than ≤6.5 g/dL calves. Body barrel
The results of linear regression analysis between TSP and calf
was greater in ≥7.0 g/dL calves than ≤6.5 g/dL calves, but 6.6–6.9 g/dL
growth performance showed that for each unit increase of TSP, the
was not different from ≥7.0 to ≤6.5 calves. Moreover, increasing TSP
final weight of the calf increased by 6.53 kg (CI: 3.86–7.91; p < 0.001),
increased withers height and hip height.
and ADG increased by 23 g/day (CI: 16.9–26.8; p = 0.04, Table 2).
Moreover, odds ratio for pneumonia between birth and weaning
As shown in Table 3, calves with TSP >6.5 g/dL at 24-h had greater
decreased as TSP increased (Table 5). The TSP concentration at 24-
BW at 30 (p = 0.001) and 60 (p = 0.001) day of life than calves with TSP
h had no significant effect on the incidence risk of diarrhoea in dairy
≤6.5 g/dL at 24-h. Furthermore, ADG during 1–30 and 1–60 days of
calves.
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2233
AGHAKHANI ET AL.
AGHAKHANI ET AL.
TA B L E 3 Least squares means (± SE) for the effects of total serum protein at 24 h of life on starter feed intake, average daily gain, feed
efficiency and body weight of dairy calves.
total serum protein at 24 h of life (g/dL)
≤6.5
Items
≥7.0
6.6–6.9
p Value
Birth body weight (kg)
38.7 ± 0.45
39.4 ± 0.53
39.9 ± 0.53
0.11
Body weight at day 30 (kg)
45.63 ± 0.49b
49.70 ± 0.50a
50.20 ± 0.56a
0.001
Body weight at day 60 (kg)
69.31 ± 0.90b
71.38 ± 1.04a
72.83 ± 1.02a
0.001
1–30 days
220.6 ± 16.7c
355.9 ± 19.2b
373.1 ± 18.2a
0.001
31–60 days
754.7 ± 25.4
b
723.5 ± 28.9
b
789.5 ± 29.9
a
0.04
1–60 days
505.0 ± 15.0c
539.5 ± 17.0b
563.7 ± 17.0a
0.04
1–30 days
461.4 ± 14.2b
456.1 ± 16.6b
536.5 ± 15.0a
0.003
31–60 days
2067.9 ± 33.0b
2073.5 ± 39.0b
2282.0 ± 36.0a
0.001
1–60 days
1264.6 ± 18.4
1264.5 ± 21.9
1409.0 ± 20.9
0.001
Average daily gain (g/day)
Starter feed intake (g/day)
a-c
b
b
a
Means within a row with different superscripts are significantly different (p < 0.05).
TA B L E 4
days of life.
Least squares means (± SE) for the effects of total serum protein at 24 h on body structures measurements (cm) of dairy calves at 60
Total serum protein at 24 h (g/dL)
Items
≤6.5
Heart girth
96.32 ± 0.61
≥7.0
6.6–6.9
b
98.81 ± 0.41
a
108.10 ± 0.92
ab
p Value
99.82 ± 0.68
a
0.001
109.61 ± 0.89
a
0.001
Body barrel
106.07 ± 0.7
Withers height
84.21 ± 0.40c
85.94 ± 0.46b
87.74 ± 0.44a
0.001
Hip height
88.88 ± 0.42
c
91.09 ± 0.49
b
92.57 ± 0.47
0.003
Hip width
14.42 ± 0.16b
16.71 ± 0.19a
16.90 ± 0.18a
0.01
Body length
51.61 ± 0.40
53.08 ± 0.46
53.73 ± 0.44
0.001
a-c
b
b
a
a
a
Means within a row with different superscripts are significantly different (p < 0.05).
TA B L E 5 Estimated odds ratios (95% CI) for the effects of total serum protein at 24 h on diarrhoea and pneumonia of dairy calves during first
60 days of life.
Total serum protein at 24 h (g/dL)
≤6.5
6.6–6.9
≥7.0
p Value
Incidence risk (%)
55.17
55.80
50.0
0.42
OR (± CI)
Reference
0.98 (0.67–1.19)
0.78 (0.50–1.21)
Incidence risk (%)
10.34a
3.42b
1.60c
OR (± CI)
Reference
0.13 (0.04–0.47)
0.05 (0.01–0.20)
Disorders
Diarrhoea
Pneumonia
a-c
4
0.001
Means within a row with different superscripts are significantly different (p < 0.05).
DISCUSSION
tural growth and health in preweaning dairy calves. This study demonstrated that TSP concentrations at 24-h <6.5 g/dL were associated with
The objective of this study was to investigate the association between
increased calf morbidity and reduced ADG, BW, structural growth and
TSP at 24-h and growth performance, starter feed intake, body struc-
starter feed intake during the preweaning period. Furthermore, these
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2234
results suggested that TSP >6.5 g/dL could be considered a new base-
gut fill and increased weights of gastrointestinal tissues not the frame
line for future analyses. In the present study, the TSP concentrations
size of body (Khan et al., 2011). Calves are expected to increase in BW
were measured by a refractometer. Many articles used refractome-
concomitantly with structural growth, and skeletal growth is equally
ters for measuring the TSP (Cuttance et al., 2019; Hue, Williams, et al.,
important function to consider because those body dimensions are not
2021; Vogels et al., 2013; Hue, Skirving, et al., 2021). Hue, Williams
often influenced by body condition, degree of fatness or gut fill (Hein-
et al. (2021) reported that serum protein refractometer measurements
richs et al., 1992). Because 50% of withers height increase occurs in the
predicted serum IgG level with high accuracy, providing an on-farm test
first 6 months of life (Kertz et al., 1998), we anticipated that the calves
to determine that calves have received sufficient passive immunity and
with greater TSP g/dL would gain faster than calves with TSP <6.5 g/dL
colostrum components.
in both BW and frame size. Although mature body size is determined
The TSP concentration at 24-h positively influenced days 30 and 60
by genetic potential, but diet and health status can result in animals
BW, day 60 body structure growth and ADG from birth to day 60. These
achieving that genetic potential earlier or being retarded in growth
results suggest that passive transfer status significantly affects growth
and never achieving their maximal mature size (Owens et al., 1993).
performance during the first month of life (Mastellone et al., 2011). In
Thus, the increased structural growth of calves with TSP greater than
agreement with our finding, Mastellone et al. (2011) detected signifi-
6.5 g/dL might be the result of additional energy and nutrients available
cant linear associations between serum Ig concentration at 24-h and
for skeletal deposition due to the increase in DMI and these calves may
BW at day 30 and ADG from birth to day 30 in buffalo calves. Moreover,
have the potential to achieve structural maturity at a younger age.
a significant association was indicated between serum IgG concentra-
Calves fed adequate colostrum immunoglobulin may develop and
tion after birth with BW and ADG during the first 21 (Elsohaby et al.,
grow normally, as opposed to calves with failure of transfer of pas-
2019) and 180 (Robison et al., 1988) days of life in dairy calves. More-
sive immunity, which have decreased nutrient utilization and reduced
over, Cuttance et al. (2018) showed that the weaning weights increased
feed intake (Colditz, 2004; Massimini et al., 2007). A meta-analysis by
by 0.4 kg for every 1.0 g/dL increase in TSP concentration. Stefańska
Soberon et al. (2012) found that every kg increase in preweaning ADG
et al. (2021) reported that BW was associated with initial TSP con-
and could increase the first lactation milk yield by 1550 kg. It could be
centration between 24 and 48 h after birth, and calves with greater
hypothesized that manipulation of heifer TSP level may offer a viable
TSP had greater BW and ADG until day 450 of life. Furman-Fratczak
method of increasing first lactation milk yield through greater starter
et al. (2011) stated that TSP levels did not affect ADG for the first 6
feed intake, ADG and body structural growth during the preweaning
months, but claves with greater TSP levels had greater ADG between
period. In agreement with our results, Stefańska et al. (2021) showed
12 and 15 months of life and achieved BW allowing first insemina-
that the initial TSP concentration of dairy heifers was associated with
tion 17 day sooner. The increase in ADG and BW of calves possibly
greater withers height and lower age at first oestrus, artificial insem-
is attributed to greater starter feed intake in the current study. Thus,
ination service, pregnancy and calving and improvement actual and
improving colostrum management practices in dairy farms and greater
energy-corrected milk during first lactation.
TSP in calves could increase starter feed intake and ADG. Starter feed
Calfhood diseases have a major impact on the economic viability of
intake is an important factor for ruminal development and minimizing
dairy cow operations, due to the direct costs of calf losses and treat-
weaning BW slump and stress, and for adapting to future solid diets,
ment and the long-term effects on performance. The lower incidence
which could also directly influence future performance (Silva et al.,
of diseases due to greater TSP concentration was expected because of
2019). Moreover, colostrum is a source of hormones and growth fac-
the great impact of colostrum-derived immune cells on calves’ health.
tors, including insulin, IGF-I, IGF-II, epidermal growth factor, growth
Many of non-immunoglobulin factors in colostrum (i.e. cytokines, GH
hormone, adiponectin and leptin (Bach, 2012). These factors promote
and IGF-1) might have interacted with Ig concentration or acted
the development of the gastrointestinal tract and the production of
directly to influence the growth response or to advance the immune
digestive enzymes (Guilloteau et al., 1997). Therefore, the adequacy
and metabolic systems of the dairy calves (Hagiwara et al., 2000; Reber
of colostrum and IgG intake has both short- and long-term effects on
et al., 2005). The same significant association was reported in previ-
dairy calves (Shivley et al., 2018) and probably influence their future
ous studies (Nocek et al., 1984; Robison et al., 1988; Virtala et al.,
growth rate, fertility and milk production. On the other hand, it was
1996). Cuttance et al. (2018a) reported that calves with TSP <5.2 g/dL
reported that ADG reduced by 0.067 kg/day in calves experienced calf-
had 1.68 times higher odds of experiencing a farmer-recorded ani-
hood respiratory disease (Buczinski et al., 2021) and calves with lower
mal health event between birth and weaning. In agreement with our
TSP concentration experienced more pneumonia in the current study.
results, Donovan et al. (1998) and Stefańska et al. (2021) noted TSP
To our knowledge, this is the first experiment that examines the
was not associated with incidence, age of onset or severity of diar-
effect of TSP at 24-h on preweaning starter feed intake and body struc-
rhoea. However, pneumonia was strongly associated with TSP during
tural growth. Calves fed greater starter feed received more energy
the first 6 months (Donovan et al., 1998). Virtala et al. (1996) reported
and protein, resulting in greater ADG and body structure. Generally,
that each additional week of pneumonia reduced total BW gain and
starter feed is an important part of a preweaned calf’s diet, and the
total height gain during the first 3 months of life by 0.8 kg and 0.2 cm,
aim is that the calf is consuming enough starter to sustain a good ADG
respectively. Moreover, higher mean haptoglobin levels and higher
and body growth during the preweaning period. However, there is a
intensity and frequency of respiratory and gastrointestinal tract mor-
common concern that an increase in BW can be attributed to greater
bidity were observed in the calves with lower Ig levels at 30–60 h
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2235
AGHAKHANI ET AL.
AGHAKHANI ET AL.
of life (Furman-Fratczak et al., 2011). An increase in haptoglobin con-
ETHICS STATEMENT
centration is commonly related to the intensity of an inflammatory
Guidelines for the care and use of animals were approved by the Iranian
reaction (Heegaard et al., 2000). Probably calves with greater TSP have
Council of Animal Care (1995). The authors confirm that the ethical
a greater capacity to inactivate pathogenic invasion and mount an ear-
policies of the journal, as noted on the journal’s author guidelines page,
lier response than calves with lower TSP; the latter must mount an
have been adhered to and the appropriate ethical review committee
acquired humoral immune response for defence (Elsohaby et al., 2019).
approval has been received. The authors confirm that they have fol-
Prevention of diseases (such as pneumonia) in the early life of dairy
lowed EU standards for the protection of animals used for scientific
calves by increasing the TSP level may improve ADG and structural
purposes.
growth of calves. Together, our results and previous studies indicate
that strategies to improve calf immunity and increase TSP lead to bet-
DATA AVAILABILITY STATEMENT
ter animal health during the preweaning period, irrespective of the
The data that support the findings of this study are available from the
dairy management system.
corresponding author upon reasonable request.
The initial feeding (colostrum and transitional milk quality and quantity) is an important factor in calf performance and health. In the
ORCID
present study, the calves received their dam’s colostrum at the rate of
Majid Toghyani
https://orcid.org/0000-0003-0470-856X
10% of their BW. In the following, the calves received similar transi-
Hassan Rafiee
https://orcid.org/0000-0002-4230-2598
tion milk, whole milk and the starter feed, and it could be noted that
the most important factor affecting the difference in TSP level was
PEER REVIEW
the quality of colostrum consumed. The colostrum’s IgG concentration
The peer review history for this article is available at https://publons.
ranged from 4.52 to 11.65 g/dL. In agreement, Immler et al. (2022)
com/publon/10.1002/vms3.1203.
and Turini et al. (2020) reported TSP increased in association with
an increase in the Brix percentage of the colostrum administered to
REFERENCES
the calves and calves being fed colostrum with higher Brix values had
Bach, A. (2012). Optimizing performance of the offspring: Nourishing and
managing the dam and postnatal calf for optimal lactation, reproduction,
and immunity. Journal of Animal Science, 90, 1835–1845.
Buczinski, S., Achard, D., & Timsit, E. (2021). Effects of calfhood respiratory
disease on health and performance of dairy cattle: A systematic review
and meta-analysis. Journal of Dairy Science, 104, 8214–8227.
Colditz, I. G. (2004). Some mechanisms regulating nutrient utilisation in
livestock during immune activation: An overview. Australian Journal of
Experimental Agriculture, 44, 453–457.
Cuttance, E. L., Mason, W. A., Laven, R. A., & Phyn, C. V. C. (2018). The
relationship between failure of passive transfer and mortality, farmerrecorded animal health events and body weights of calves from birth
until 12 months of age on pasture-based, seasonal calving dairy farms in
New Zealand. The Veterinary Journal, 236, 4–11.
Cuttance, E. L., Regnerus, C., & Laven, R. A. (2019). A review of diagnostic
tests for diagnosing failure of transfer of passive immunity in dairy calves
in New Zealand. New Zealand Veterinary Journal, 67, 277–286.
Denise, S. K., Robison, J. D., Stott, G. H., & Armstrong, D. V. (1989). Effects
of passive immunity on subsequent production in dairy heifers. Journal of
Dairy Science, 72, 552–554.
Donovan, G. A., Dohoo, I. R., Montgomery, D. M., & Bennett, F. L. (1998).
Associations between passive immunity and morbidity and mortality
in dairy heifers in Florida, USA. Preventive Veterinary Medicine, 34, 31–
46.
Elsohaby, I., Cameron, M., Elmoslemany, A., McClure, J. T., & Keefe, G.
(2019). Effect of passive transfer of immunity on growth performance
of preweaned dairy calves. Canadian Journal of Veterinary Research, 83,
90–96.
Furman-Fratczak, K., Rzasa, A., & Stefaniak, T. (2011). The influence of
colostral immunoglobulin concentration in heifer calves’ serum on their
health and growth. Journal of Dairy Science, 94, 5536–5543.
Godden, S. M., Lombard, J. E., & Woolums, A. R. (2019). Colostrum management for dairy calves. Veterinary Clinics of North America: Food Animal
Practice, 35, 535–556.
Guilloteau, P., Le Huërou-Luron, I., Chayvialle, J. A., Toullec, R., Zabielski, R.,
& Blum, J. W. (1997). Gut regulatory peptides in young cattle and sheep.
Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine,
44, 1–23.
greater TSP concentration.
5
CONCLUSIONS
Our results suggest that TSP at 24-h had positive effects on BW, ADG,
starter feed intake, body structural growth and lower pneumonia during the preweaning period. Moreover, TSP at 24-h is a significant source
of variation in growth performance and morbidity during the preweaning period. Calves with TSP >6.5 g/dL had greater starter feed intake
and lower pneumonia incidence, leading to greater ADG and body
structural growth during the preweaning period. Our results indicate
that strategies to improve calf immunity and increase TSP lead to better animal health during the preweaning period. Moreover, our findings
suggested that TSP >6.5 g/dL could be considered a new baseline for
future analyses.
AUTHOR CONTRIBUTIONS
Conceptualization; formal analysis; methodology: Mitra Aghakhani. Conceptualization; funding acquisition; investigation; supervision: Amir Davar
Foroozandeh Shahraki. Investigation; supervision: Seyed Nouroldin
Tabatabaei and Majid Toghyani. Methodology: Erfaneh Moosavi-Zadeh.
Writing original draft; writing review and editing: Hassan Rafiee.
ACKNOWLEDGEMENTS
The researchers would like to express their thanks to all people who
assisted them in accomplishment of this research.
CONFLICT OF INTEREST STATEMENT
The authors declare that there are not any conflicts of interest.
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2236
Habibi, Z., Karimi-Dehkordi, S., Kargar, S., & Sadeghi, M. (2020). Grain source
and chromium supplementation: Effects on health metabolic status and
glucose-insulin kinetics in Holstein heifer calves. Journal of Dairy Science,
102, 8941–8951.
Hagiwara, K., Kataoka, S., Yamanaka, H., Kirisawa, R., & Iwai, H. (2000).
Detection of cytokines in bovine colostrum. Veterinary Immunology and
Immunopathology, 76, 183–190.
Hassig, M., Stadler, T., & Lutz, H. (2007). Transition from maternal to endogenous antibodies in newborn calves. Veterinary Record, 160, 234–235.
Heegaard, P. M. H., Godson, D. L., Toussaint, M. J. M., Tjørnehøj, K., Larsen,
L. E., Viuff, B., & Rønsholt, L. (2000). The acute phase response of haptoglobin and serum amyloid A (SAA) in cattle undergoing experimental
infection with bovine respiratory syncytial virus. Veterinary Immunology
and Immunopathology, 77, 151–159.
Heinrichs, A. J., Rogers, G. W., & Cooper, J. B. (1992). Predicting body weight
and wither height in Holstein heifers using body measurements. Journal
of Dairy Science, 75, 3576–3581.
Hue, D. T., Williams, J. L., Petrovski, K., & Bottema, C. D. K. (2021). Predicting
colostrum and calf blood components based on refractometry. Journal of
Dairy Research, 88, 194–200.
Hue, D. T., Skirving, R., Chen, T., Williams, J. L., Bottema, C. D. K., & Petrovski,
K. (2021). Colostrum source and passive immunity transfer in dairy bull
calves. Journal of Dairy Science, 104, 8164–8176.
Immler, M., Büttner, K., Gärtner, T., Wehrend, A., & Donat, K. (2022). Maternal impact on serum immunoglobulin and total protein concentration in
dairy calves. Animals, 12, 755–769.
Iranian Council of Animal Care. (1995). Guide to the care and use of
experimental animals (Vol. 1). Isfahan University of Technology.
Kelly, G. (2003). Bovine colostrums: A review of clinical uses. Alternative
Medicine Review, 8, 78–394.
Kertz, A. F., Barton, B. A., & Reutzel, L. F. (1998). Relative efficiencies of
wither height and body weight increase from birth until first calving in
Holstein cattle. Journal of Dairy Science, 81, 1479–1482.
Khan, M. A., Weary, D. M., & von Keyserlingk, M. A. G. (2011). Hay intake
improves performance and rumen development of calves fed higher
quantities of milk. Journal of Dairy Science, 94, 3547–3553.
Lombard, J., Urie, N., Garry, F., Godden, S., Quigley, J., Earleywine, T.,
McGuirk, S., Moore, D., Branan, M., Chamorro, M., Smith, G., Shivley, C.,
Catherman, D., Haines, D., Heinrichs, A. J., James, R., Maas, J., & Sterner,
K. (2020). Consensus recommendations on calf- and herd-level passive
immunity in dairy calves in the United States. Journal of Dairy Science,
103, 7611–7624.
Manriquez, D., Valenzuela, H., Paudyal, S., Velasquez, A., & Pinedo, P. J.
(2018). Effect of aluminized reflective hutch covers on calf health and
performance. Journal of Dairy Science, 101, 1464–1477.
Massimini, G., Mastellone, V., Britti, D., Lombardi, P., & Avallone, L. (2007).
Effect of passive transfer status on preweaning growth performance in
dairy goat kids. Journal of the American Veterinary Medical Association, 231,
1873–1877.
Mastellone, V., Massimini, G., Pero, M. E., Cortese, L., Piantedosi, D.,
Lombardi, P., & Avallone, L. (2011). Effects of passive transfer status
on growth performance in buffalo calves. Asian-Australasian Journal of
Animal Sciences, 24, 952–956.
McGuirk, S. M., & Collins, M. (2004). Managing the production, storage, and
delivery of colostrum. Veterinary Clinics of North America: Food Animal
Practice, 20, 593–603.
Mirzakhani, A., Ghorbani, G. R., Sadeghi-Sefidmazgi, A., Rafiee, H., &
Drackley, J. K. (2021). Effects of starter protein content and alkali processing of wheat straw on growth, ruminal fermentation, and behavior in
Holstein calves. Journal of Dairy Science, 104, 3098–3108.
Morrill, K. M., & Tyler, H. D. (2012). Two methods to determine IgG
concentration in calf serum. Animal Industry Report, 658, ASL R2708.
Nocek, J. E., Braund, D. G., & Warner, R. G. (1984). Influence of neonatal colostrum administration, immunoglobulin, and continued feeding of
colostrum on calf gain, health, and serum protein. Journal of Dairy Science,
67, 319–333.
Owens, F. N., Dubeski, P., & Hanson, C. F. (1993). Factors that alter the
growth and development of ruminants. Journal of Animal Science, 71,
3138–3150.
Reber, A. J., Hippen, A. R., & Hurley, D. J. (2005). Effects of the ingestion
of whole colostrum or cell-free colostrum on the capacity of leukocytes
in newborn calves to stimulate or respond in one-way mixed leukocyte
cultures. American Journal of Veterinary Research, 66, 1854–1860.
Robinson, J. D., Stott, G. H., & De Nise, S. K. (1988). Effects of passive immunity on growth and survival in the dairy heifer. Journal of Dairy Science, 71,
1283–1287.
Shearer, J., Mohammed, H. O., Brenneman, J. S., & Tran, T. Q. (1992). Factors
associated with concentrations of immunoglobulins in colostrum at the
first milking post-calving. Preventive Veterinary Medicine, 14, 143–154.
Shivley, C. B., Lombard, J. E., Urie, N. J., Haines, D. M., Sargent, R., Kopral,
C. A., Earleywine, T. J., Olson, J. D., & Garry, F. B. (2018). Preweaned
heifer management on US dairy operations: Part II. Factors associated
with colostrum quality and passive transfer status of dairy heifer calves.
Journal of Dairy Science, 101, 9185–9198.
Silva, A. L., DeVries, T. J., Tedeschi, L. O., & Marcondes, M. I. (2019). Development of equations, based on milk intake, to predict starter feed intake of
preweaned dairy calves. Animal, 13, 83–89.
Soberon, F., Raffrenato, E., Everett, R. W., & van Amburgh, M. E. (2012).
Preweaning milk replacer intake and effects on long-term productivity
of dairy calves. Journal of Dairy Science, 95, 783–793.
Stefańska, B., Gąsiorek, M., & Nowak, W. (2021). Short- and long-term
effects of initial serum total protein, average starter feed intake during the last week of the preweaning period, and rearing body gain on
primiparous dairy heifers’ performance. Journal of Dairy Science, 104,
1645–1659.
Thornhill, J. B., Krebs, G. L., & Petzel, C. E. (2015). Evaluation of the Brix
refractometer as an on-farm tool for the detection of passive transfer of
immunity in dairy calves. Australian Veterinary Journal, 93, 26–30.
Turinia, L., Conte, G., Bonelli, F., Sgorbinia, M., Madrigalia, A., & Mele, M.
(2020). The relationship between colostrum quality, passive transfer of
immunity and birth and weaning weight in neonatal calves. Livestock
Science, 238, 104033.
Tyler, J. W., Hancock, D. D., Parish, S. M., Rea, D. E., Besser, T. E., Sanders,
S. G., & Wilson, L. K. (1996). Evaluation of 3 assays for failure of passive
transfer in calves. Journal of Veterinary Internal Medicine, 10, 304–307.
Virtala, A. M., Mechor, G. D., Gröhn, Y. T., & Erb, H. N. (1996). The effect
of calfhood diseases on growth of female dairy calves during the first 3
months of life in New York State. Journal of Dairy Science, 79, 1040–1049.
Vogels, Z., Chuck, G. M., & Morton, J. M. (2013). Failure of transfer of passive
immunity and agammaglobulinaemia in calves in south-west Victorian
dairy herds: Prevalence and risk factors. Australian Veterinary Journal, 91,
150–158.
Windeyer, M. C., Leslie, K. E., Godden, S. M., Hodgins, D. C., Lissemore, K. D.,
& LeBlanc, S. J. (2014). Factors associated with morbidity, mortality, and
growth of dairy heifer calves up to 3 months of age. Preventive Veterinary
Medicine, 113, 231–240.
How to cite this article: Aghakhani, M., Shahraki, A. D. F.,
Tabatabaei, S. N., Toghyani, M., Moosavi-Zadeh, E., & Rafiee, H.
(2023). 24-Hour postnatal total serum protein concentration
affects the health and growth performance of female Holstein
dairy calves. Veterinary Medicine and Science, 9, 2230–2237.
https://doi.org/10.1002/vms3.1203
20531095, 2023, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/vms3.1203 by Cochrane Mexico, Wiley Online Library on [26/10/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2237
AGHAKHANI ET AL.