J. Dairy Sci.

106:7043–7055
https://doi.org/10.3168/jds.2022-22448
© 2023, The Authors. Published by Elsevier Inc. and Fass Inc. on behalf of the American Dairy Science Association®.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Association between transfer of passive immunity, health,

and performance of female dairy calves from birth to weaning
F. Sutter, P. L. Venjakob, W. Heuwieser,* and S. Borchardt
Clinic for Animal Reproduction, Faculty of Veterinary Medicine, Freie Universität Berlin, 14163 Berlin, Germany

ABSTRACT had diarrhea, and 31 (0.9%) and 957 (27.9%) suffered

from omphalitis and pneumonia during the first 90 d
The objective of this observational study was to of life, respectively. Overall, the morbidity during the
compare calf health, average daily weight gain, and preweaning period was 32.6% (n = 1,118), and the
calf mortality considering the proposed categories of mortality was 3.1% (n = 107). The ADG was 0.90 ±
transfer of passive immunity (TPI) by the consensus 0.15 kg with a range of 0.32 to 1.52 kg. The Cox regres-
report of Lombard et al. (2020). The consensus report sion model showed that calves suffering from poor TPI
defines 4 categories of passive immunity (excellent, tended toward a greater hazard risk (HR) for diarrhea
good, fair, and poor) of calves obtained after colostrum (HR = 1.57, 95% CI: 0.92–2.69) compared with calves
ingestion. The association between the 4 TPI categories with excellent TPI. Calves suffering from TPI had a
was analyzed on calf health (i.e., hazards for morbidity greater HR for pneumonia (HR = 2.00, CI: 1.53–2-
and mortality), and average daily weight gain (ADG) 61), overall morbidity (HR = 1.99, CI: 1.56–2.55),
of female Holstein Friesian calves during the first 90 and mortality (HR = 2.47, CI: 1.25–4.86) in contrast
d of age. A further aim of this study was to examine to excellent TPI. Furthermore, calves with good and
the effects of calving-related factors, such as dystocia fair TPI had significantly greater HR for pneumonia
or winter season, on TPI status. We hypothesized that (good TPI: HR = 1.35, CI: 1.15–1.59; fair TPI: HR =
calves with excellent TPI have greater ADG, lower risks 1.41, CI: 1.20–1.65) and overall morbidity (good TPI:
for infectious diseases such as neonatal diarrhea, pneu- HR = 1.26, CI: 1.09–1.47; fair TPI: HR = 1.32, CI:
monia, and omphalitis, and lower mortality rates. This 1.14–1.53) compared with the excellent TPI category.
observational study was conducted from December 2017 Average daily weight gain during the first 60 d of life
to March 2021. Blood was collected from 3,434 female was associated with TPI categories. Calves with excel-
Holstein Friesian dairy calves from 1 commercial dairy lent and good TPI status had ADG of 0.90 ± 0.01 kg/d
farm. All female calves aged 2 to 7 d were assessed and 0.92 ± 0.01 kg/d (mean ± SE), respectively. The
for TPI status by determination of total solids (TS) ADG of calves with fair TPI status was 0.89 ± 0.01
in serum via Brix refractometry by the farm personnel kg/d, and calves suffering from poor TPI had 0.86 ±
once a week. Passive immunity was categorized accord- 0.01 kg/d. Average daily weight gain differed in calves
ing to Lombard et al. (2020) with excellent (≥9.4% with poor TPI compared with the other categories. Fair
Brix), good (8.9–9.3% Brix), fair (8.1–8.8% Brix), or and excellent TPI differed additionally from good TPI.
poor TPI (<8.1% Brix). For the analysis of ADG and We found no statistical difference between the TPI cat-
calving ease 492 or 35 calves had to be excluded due egories fair and excellent. In conclusion, poor TPI was
to missing data. The distribution of calves according associated with higher morbidity and mortality during
to TPI categories was as follows: 4.8% poor (n = 166), the first 90 d of life. Furthermore, calves with fair, good
29.5% fair (n = 1,012), 28.3% good (n = 971), and or excellent TPI had greater ADG.
37.4% excellent (n = 1,285). From the calving-related Key words: categories of passive immunity, neonatal
factors, parity of the dam, calving ease, birth month, calves, average daily weight gain, hazard for disease
calving assistance by different farm personnel, and day
of life for TPI assessment were significantly associated
INTRODUCTION
with TS concentration. Out of 3,434 calves, 216 (6.3%)
Sound evidence suggests that adequate supply of
colostrum to the neonatal calf after birth is crucial for
its passive immunity and essential for calf health (Cut-
Received June 27, 2022.
Accepted March 22, 2023. tance et al., 2018; Lora et al., 2018; Godden et al.,
*Corresponding author: w.heuwieser@​fu​-berlin​.de 2019). During gestation, the bovine cotyledonary syn-

7043
 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7044

epitheliochorial placenta impedes the transfer of mater- IgG categories: excellent (≥25.0 g/L; ≥9.4% Brix),
nal immunoglobulins (Ig) from the dam to the fetus, good (18.0–24.9 g/L; 8.9–9.3% Brix), fair (10.0–17.9
and the calves are born immunonaive (Barrington and g/L; 8.1–8.8% Brix), and poor (<10 g/L; <8.1% Brix;
Parish, 2001; Furukawa et al., 2014; Fischer-Tlustos Lombard et al., 2020). Regarding the herd level, >40%
et al., 2021). Therefore, the intestinal absorption of of the calves should achieve the excellent category, and
maternal Ig, especially IgG, via colostrum is essential 30%, 20%, and <10% of calves should meet the good,
for successful passive transfer in neonatal dairy calves fair, and poor TPI categories, respectively. This new
(Weaver et al., 2000; Godden et al., 2009; Godden et classification has the potential to contribute a reduc-
al., 2019). Because the calf is dependent on the mater- tion of morbidity in dairy calves; thus the risks of pre-
nal Ig, the timely delivery of high-quality colostrum in weaning morbidity and mortality and among these TPI
a sufficient quantity is necessary for a high intestinal categories need to be compared.
absorption rate during the first 24 h after birth. This The objective of this observational study was to
process is known as transfer of passive immunity (TPI) compare calf health (i.e., hazards for morbidity and
and it is necessary to protect the calf against pathogens mortality) and ADG between the proposed recommen-
and common diseases (Weaver et al., 2000; Godden et dations for TPI assessment by the consensus report
al., 2009; Godden et al., 2019). Furthermore, an ap- of Lombard et al. (2020) of female Holstein Friesian
propriate colostrum volume for first feeding (~10% of calves during the first 90 d of age. In addition, we
bodyweight, 4 L in Holstein Friesian calves) positively aimed to evaluate the effects of calving-related factors
affects the calf’s metabolism (i.e., reduced mortality (e.g., dystocia, winter season, farm employee providing
rates, higher ADG; Blum and Hammon, 2000; Fischer- calving assistance and neonatal care) on TPI status.
Tlustos et al., 2021) and may influence its performance We hypothesized that calves with excellent TPI have
as an adult dairy cow (i.e., reduced age at first calving; greater ADG, lower risks for infectious diseases such
Faber et al., 2005). This is related to other components as neonatal diarrhea, pneumonia and omphalitis, and
of colostrum. Important non-immunoglobulin immune lower mortality rates during the first 90 d of age. Fur-
factors, termed milk-borne factors (e.g., insulin-like thermore, we hypothesized that calving-related factors,
growth factor I, epidermal growth factor), are provided such as dystocia or the winter season, negatively affect
by colostrum feeding, as well as energy, fluid intake, the TPI status.
and heat support for the thermoregulation (Blum and
Hammon, 2000; Bagnell et al., 2009; Silva and Machado MATERIALS AND METHODS
Bittar, 2019; Fischer-Tlustos et al., 2021).
Methods for TPI assessment can be performed in Dairy Farm and Animal Enrollment
calves aged 24 h to 7 d by direct measurement of IgG
or indirect measurement of total protein or TS in calf This observational study was conducted from Decem-
serum or plasma. During the last decades the standard ber 2017 to March 2021 on a commercial dairy farm in
for categorizing dairy calves with successful passive im- Mecklenburg-Vorpommern, Germany. Because all the
munity or failed transfer of passive immunity (FTPI) required material was obtained during routine farm
was defined as serum IgG concentrations above or be- management practices to monitor poor TPI, calf health,
low 10 mg/mL in 24- to 48-h-old calves, respectively and heifer development, an exemption from protocol
(Weaver et al., 2000; McGuirk and Collins, 2004; God- review of the Institutional Animal Care and Use Com-
den, 2008). This threshold for serum IgG helped to re- mittee of the Freie Universität Berlin was granted. The
duce calf mortality in heifer calves (USDA, 1996, 2018). farm owned approximately 2,500 Holstein cows with
Interestingly, calf morbidity has still not declined in an average annual milk yield of 11,000 kg/cow. Heifers
the United States (USDA, 1994, 2018; Lombard et al., and cows were housed in a naturally ventilated transi-
2020). According to Lombard et al. (2020), new rec- tion management facility consisting of 4 freestall pens,
ommendations for TPI assessment could improve this providing cubicles with sand bedding and ad libitum
pending problem. These recommendations were made access to feed and water from drying off to the first 20
based on conference calls with various academic and DIM (36 heifer cubicles and 144 cow cubicles). All cows
calf health professionals to discuss different publications were vaccinated during the dry period, and prepartum
and the data from the NAHMS study (Dairy 2014, calf heifers were vaccinated before the first calving against
component; Urie et al., 2018a,b). Groups of calf ex- Escherichia coli, bovine rota- and coronavirus (Rotavec
perts were established to evaluate the data and identify Corona, MSD Animal Health, Intervet Deutschland
whether changes to passive immunity standards were GmbH, Unterschleißheim, Germany) to improve colos-
necessary to reduce morbidity and potentially mortal- trum quality. The vaccination was carried out approxi-
ity. New TPI suggestions were made based on 4 serum mately 6 wk before calving.
Journal of Dairy Science Vol. 106 No. 10, 2023
 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7045

Prepartum cows and heifers were monitored every buckets. Milk replacer (Pro Elite 60, Dairytop, Beilen,
30 min to detect signs of imminent parturition (Lange the Netherlands; 24% CP, 18.5% crude fat, and 60%
et al., 2017). The dams were moved into an individual skim milk powder) was added to increase milk solids to
maternity pen (3.5 m2), when the amniotic sac or calf reach 170 g/L. The quantity fed was 3.5 L twice daily
feet were visible outside the vulva. A manual vaginal in the first week of life, 2 × 4 L from d 7 to d 10, and 2
examination was conducted in every animal transferred × 4.5 L from d 10 until 60 d of age. Afterward the milk
to the maternity pen to assess dilatation of the vulva volume was reduced stepwise during 24 d until 1 L once
and cervix, as well as position, posture, presentation, daily was fed. Weaning finally ended at 90 d of age. In
and vitality of the calf. Calving assistance was provided the third week of life, female calves were reallocated
to reduce calf losses, if the cow had not delivered the into 35-m2 group housing pens (10 calves/pen) until
calf 1 h after moving the cow to the maternity pen weaning. Each group was fed via a calf group feeder
(Schuenemann et al., 2011). Intensity of calving assis- equipped with 10 teats (Milk Bar 10, Milk Bar, Olden-
tance was recorded on a 4-point scale (1 = no assis- burg, Germany). During group housing the calves had
tance; 2 = assistance by 1 person; 3 = assistance by at access to TMR consisting of a mixture of concentrate,
least 2 persons; 4 = cesarean section). Postpartum cows chopped straw, soy meal, molasses, and chalk.
were milked 3 times daily (0600 h, 1400 h, and 2200 Weighing was performed directly after birth and at
h). A detailed description of the calving management d 60 with an electronic scale (WA200 mobile platform
and the first milking after calving has been described scale, Meier-Brakenberg GmbH & Co. KG, Extertal,
previously (Sutter et al., 2019). Germany).
Immediately after birth, calves were separated from Calves were considered clinically healthy when vis-
their dams and were weighed with an electronic scale ible signs of disease were not observed. Appearance of
(WA200 mobile platform scale, Meier-Brakenberg disease was monitored once daily by the farm person-
GmbH & Co. KG, Extertal, Germany) before placing nel using the calf health scoring chart created by the
them into a hutch (1.5 × 1 m) bedded with fresh straw University of Wisconsin. The chart applies validated
for the first 24 h following birth. All newborn calves methods for fecal scoring (McGuirk, 2008), respiratory
had their navels dipped using a 10% tincture of iodine screening (McGuirk and Peek, 2014), and detection
solution (Braunol, B. Braun Melsungen AG, Melsun- of omphalitis. Farm personnel were trained to assess
gen, Germany). Standard operating procedures were clinical signs and apply treatments according to vet-
in place for colostrum feeding and Brix refractometry. erinarian’s instructions. Neonatal diarrhea was defined
The first meal consisted of 4 L of pasteurized (Perfect as visibly loose feces of decreased consistency (Renaud
Udder, Dairy Tech Inc., Greeley, CO), pooled, high- et al., 2020). Pneumonia was defined as visibly detect-
quality colostrum (containing ≥22% Brix; Bielmann able tachypnea with nasal discharge (serous, mucous,
et al., 2010) and was fed approximately 30 min after or purulent) and presence of cough (McGuirk, 2005).
calving using an esophageal tube feeder (Dairymac Omphalitis was present when a combination of several
Drencher, Dairytop, Beilen, Netherlands). At 6 to 12 h signs was observed: clinical signs (redness, swelling, pu-
after the first meal, the female calves received another rulent discharge, painful response to palpation) in addi-
2 L of colostrum. All female calves aged 2 to 7 d were tion to fever (>39.5°C) or lack of appetence (Fordyce et
assessed for passive immunity by determination of TS al., 2018). Only cases of disease associated with treat-
in serum by the farm personnel. On average, 30 animals ment were included in the statistical analysis. Cases of
were tested per week. Calves with clinical signs of de- diarrhea were treated once daily for 3 d with 1.25 mg/
hydration were excluded from the blood testing. Blood kg i.m. danofloxacin (Advocid, Zoetis GmbH, Berlin,
withdrawal was performed by jugular vein puncture Germany). Cases of pneumonia were treated with a
once a week. Blood samples were centrifuged at 4.500 × single administration of 2.5 mg/kg i.m. tulathromycin
g for 6 min at approximately 20°C on the farm 1 to 2 h (Draxxin, Zoetis GmbH, Berlin, Germany), and cases
after collection and were directly assessed via a digital of omphalitis were treated once daily for 3 d with 15–20
Brix refractometer (Misco PA201, Misco, Solon, OH). mg i.m. procaine benzylpenicillin (Procain Penicillin G,
Calibration of the Brix refractometer was performed AniMedica International GmbH, Frankfurt, Germany).
once a week with distilled water by the farm personnel.
On d 2 of life the female calves were moved to the Data Collection and Statistical Analyses
calf barn and placed into individual pens bedded with
straw. Water and starter grain (20% CP; 6.7 MJ NE1/ All prepartum cows and heifers having singleton
kg) were provided ad libitum from d 1 and 7 of life, calves and without cesarean section were included in
respectively. The feeding protocol consisted of feeding the study. Relevant data such as date and time of par-
twice daily pasteurized whole milk using individual teat turition, sex of the calf, twin births, calving assistance
Journal of Dairy Science Vol. 106 No. 10, 2023
 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7046

and cesarean section, birth weight and following weight was the experimental unit. Each parameter considered
recordings, time of first feeding, identification number, for the mixed model was separately analyzed in a uni-
serum TS concentration (in % Brix) reflecting the TPI variate model, including the parameter as a fixed factor
status, and treatment records during the preweaning (i.e., categorical parameter) or covariate (i.e., continu-
period were obtained from the on-farm computer soft- ous parameter; Dohoo et al., 2009). Only parameters
ware (DairyCOMP 305; Valley Ag Software, Tulare, resulting in univariate models with P ≤ 0.20 were in-
CA). The data were transferred to Microsoft Excel cluded in the final mixed model. Selection of the model
(Office 2013, Microsoft Deutschland Ltd., Munich, that best fit the data was performed by testing each ef-
Germany). Passive immunity was categorized accord- fect separately in a multivariate model and finding the
ing to Lombard et al. (2020) with excellent (≥9.4% model with the lowest value for the Akaike information
Brix), good (8.9–9.3% Brix), fair (8.1–8.8% Brix), or criterion, using a backward elimination procedure that
poor TPI (<8.1% Brix). Farm personnel were blinded removed all variables with P > 0.10 from the model.
to the TPI category, though the TS result in % Brix A significant statistical difference was defined for vari-
was not blinded, as being part of the standard operat- ables between the levels of a classification when P <
ing procedure of the farm. 0.05; a statistical tendency was specified as differences
Statistical analyses were performed using SPSS for between P ≥ 0.05 and P ≤ 0.10.
Windows (version 22.0, IBM Corp., Ehningen, Ger- The initial model for TS concentration in % Brix
many). Average daily weight gain was calculated from contained the following variables as fixed effects: parity
the difference between weight at 60 d and birth weight (1, 2, and ≥3); calving ease (score 1 to 3); employee
divided by the age in days. responsible for calving, milking, and neonatal care (1
Cox proportional hazard models were used to observe to 8); birth month (1 to 12 mo); calving time during
the time to event outcomes—that is, occurrence of neo- the day (1 to 24 h); colostrum harvesting time after
natal diarrhea, omphalitis, pneumonia, overall morbid- calving (hours, continuous); time of colostrum feeding
ity (occurrence of diarrhea, omphalitis, and pneumonia after calving (minutes, continuous); calf birth weight
in total) as well as mortality—during the first 90 d of (continuous); and day of life for TPI assessment (2 to
life. Cox regression models were performed to create a 7 d).
hazard model for the TPI categories referring to the The initial models for ADG during the preweaning
disease prevalence (diarrhea, omphalitis, pneumonia, period contained the same variables as for % Brix,
and overall morbidity) and mortality during the first including TS concentration (continuous) and TPI cat-
90 d of life, respectively. The hazard model specified egories (poor, fair, good, excellent).
the time until an event (disease or mortality) occurred The initial models for disease prevalence (diarrhea,
and produced a hazard or survival function considering omphalitis, or pneumonia), overall morbidity and mor-
the different TPI categories. For the morbidity mod- tality during the preweaning period contained the same
els, calves that died before 90 d of age were censored. variables as for % Brix, including ADG (kg/d; continu-
Proportional hazard or survival assumptions were illus- ous), TS concentration (% Brix; continuous) and TPI
trated by plotting the −ln [−ln (disease or mortality)] categories (poor, fair, good, excellent). We tested all
curves for calves during the preweaning period against biologically plausible 2-way interactions. In the case of
the ln (hazard time or survival time). multiple comparisons, the P-value was adjusted using a
To evaluate the association between calving manage- Bonferroni correction.
ment (parity, calving ease, employee, colostrum har- To evaluate significant differences between ADG, dis-
vesting time, colostrum feeding time, day of TPI assess- ease prevalence (diarrhea, omphalitis, and pneumonia),
ment) and environmental factors (birth month, calving overall morbidity and mortality, and the TPI catego-
time) as calving-related factors and the TS concentra- ries (poor, fair, good, excellent) during the prewean-
tion in % Brix, a generalized linear mixed model was ing period, a one-way ANOVA was performed using
constructed using the GENLINMIXED procedure of SPSS. The dependent variable was either ADG (kg/d;
SPSS. Furthermore, 6 generalized linear mixed models continuous), disease event (diarrhea, omphalitis, and
were constructed to evaluate the association between pneumonia), and overall morbidity and mortality (cat-
TS concentration in % Brix as well as TPI category and egorical parameters), and the independent variable was
ADG (continuous parameter), disease prevalence (diar- TPI categories (poor, fair, good, excellent).
rhea, omphalitis, and pneumonia), overall morbidity,
and mortality during the preweaning period. The out- RESULTS
come variable was either ADG (continuous parameter),
diarrhea, omphalitis or pneumonia prevalence, overall From a total of 3,951 records, only 3,434 female dairy
morbidity, or mortality (categorical parameters). Calf calves were included in this observational study from
Journal of Dairy Science Vol. 106 No. 10, 2023
 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7047

December 2017 to March 2021. A total of 517 animals

Table 1. Descriptive statistics and Pearson chi squared tests for the status of transfer of passive immunity (TPI) in % Brix of female Holstein Friesian calves considering parity (n
= 3,434), calving ease (n = 3,399), ADG (n = 2,942), and disease and survival prevalence during the first 90 d of life (n = 3,434); P-value adjusted using a Bonferroni correction
were removed from the data set and excluded from the

41.5
24.0
34.6

67.5
17.0
15.5

6.3
23.0
0.9
27.9
2.7
%
statistical analysis, because TPI data were missing in
340 cases, 5 animals received a cesarean section as calv-
ing assistance, and 172 calves were twins. Furthermore,

Excellent TPI

0.90 ± 0.01b
to evaluate the association between calving assistance
as well as ADG and TPI, additional 35 (1%) and 492

198b

295b

35b
533a
308a
444a

217a

81a

11a
860c

358c
(14.3%) animals had to be excluded from the statistical
analysis because calving was not observed or ADG data
were missing, respectively.
The passive immunity of the calves classified in TPI

37.0
24.4
38.6

66.2
17.9
15.9

6.1
29.7
1.2
33.9
2.6
%
categories was represented as follows: 4.8% poor (n =
166), 29.5% fair (n = 1,012), 28.3% good (n = 971),
and 37.4% excellent TPI (n = 1,285). First colostrum

Category of passive immunity1

0.92 ± 0.01c
Good TPI
was fed at 48.3 ± 43.4 min (mean ± SD) with a range

Calving ease: score 1 = no calving assistance; score 2 = calving assistance by 1 person; score 3 = calving assistance by 2 persons.
of 8 to 431 min after calving. Calving assistance was

637b,c

153b

329b
25b
359a
237a
375a

172a

59a
288a
12a
provided in 1,210 dairy cows (score 2, n = 628; score 3,

Category of passive immunity: poor = <8.1% Brix; fair = 8.1–8.8% Brix; good = 8.9–9.3% Brix; excellent = ≥9.4% Brix.
n = 582). The average birth weight was 40.2 ± 4.7 kg.
Second weighing took place at an average age of 62.3
± 9.7 d, and the average weight was 96.4 ± 13.5 kg.

38.0
22.4
39.5

61.7
20.1
18.2

5.9
30.4
0.7
34.9
3.6
%
The ADG was 0.90 ± 0.15 kg with a range of 0.32 to
1.52 kg.
Out of 3,434 calves, 216 (6.3%) calves had diar-

0.89 ± 0.01b
rhea, and 31 (0.9%) and 957 (27.9%) calves suffered

Fair TPI
from omphalitis and pneumonia, respectively, during

36a,b
615b

181b

353b
385a
227a
400a

200a

60a
308a
7a
the first 90 d of life. Overall, the morbidity during the
preweaning period was 32.6% (n = 1,118), with 1,032
calves suffering from 1 disease (30.1%) and 86 calves
having multiple diseases (2.5%). The mortality was
34.9
21.1
44.0

46.4
23.5
30.1

9.6
39.8
0.6
47.0
6.6
%

3.1% (n = 107). Descriptive statistics for the TPI cat-

egories, parity, calving ease, and ADG, and disease and
survival prevalence are summarized in Table 1. Disease
0.86 ± 0.01a
Poor TPI

prevalence and mortality stratified by TPI category are

illustrated in Figure 1A–D.
58a
35a
73a

77a
39a
50a

16a
66a
1a
78a
11a
According to the Cox regression model, the TPI

Rows with different superscripts differ significantly (P < 0.05).

category of the dairy calves affected morbidity and
mortality. Compared with calves with excellent TPI,
P-value
0.062

<0.001

<0.001
0.326
<0.001
0.592
<0.001
0.029
calves suffering from poor TPI had a greater hazard
risk (HR) for pneumonia (HR = 2.00; P < 0.01; 95%
CI: 1.53–2.61), overall morbidity (HR = 1.99; P < 0.01;
38.9
23.5
37.6

64.4
18.5
17.1

6.3
27.9
0.9
32.6
3.1

CI: 1.56–2.55), or mortality (HR = 2.47; P < 0.01; CI:

%

1.25–4.86). We found a tendency toward a greater HR

for diarrhea (HR = 1.57; P = 0.10; CI: 0.92–2.69) for
1,335
3,434

807
1,292
3,399
2,189
628
582
2,942
216
957
31
1,118
107

calves suffering from poor TPI compared with calves

n

with excellent TPI. Furthermore, calves with good and

fair TPI had significantly greater HR for pneumonia
(good TPI: HR = 1.35, P < 0.01, CI: 1.15–1.59; fair
ADG (kg/d; mean ± SE)
in multiple comparisons

TPI: HR = 1.41, P < 0.01; CI: 1.20–1.65) and overall

morbidity (good TPI: HR = 1.26, P < 0.01, CI: 1.09–
1.47; fair TPI: HR = 1.32; P < 0.01, CI: 1.14–1.53)
Calving ease2

compared with the excellent TPI category (Figure

Pneumonia
Omphalitis
Parity ≥3

Morbidity

2A–D).
Mortality
Parity 1
Parity 2

Diarrhea
Score 1
Score 2
Score 3

Parity of the dam (P = 0.06), calving ease (P <

Parity
Item

0.01), birth month (P = 0.04), calving assistance of

a–c

Journal of Dairy Science Vol. 106 No. 10, 2023

 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7048

Figure 1. (A) Diarrhea prevalence (%) of female Holstein Friesian calves (n = 3,434) with different transfer of passive immunity categories
(poor: <8.1% Brix, n = 166; fair: 8.1–8.8% Brix, n = 1,012; good: 8.9–9.3% Brix, n = 971; excellent: ≥9.4% Brix, n = 1,285) during the first
90 d of life. Neonatal diarrhea was defined as visibly loose feces of decreased consistency. (B) Pneumonia prevalence (%) of female Holstein
Friesian calves (n = 3,434) with different categories of transfer of passive immunity during the first 90 d of life. Pneumonia was defined as visibly
detectable tachypnea with nasal discharge (serous, mucous, or purulent). (C) Morbidity rate (%) of female Holstein Friesian calves (n = 3,434)
with different categories of transfer of passive immunity during the first 90 d of life. Overall, 1,032 calves were suffering from 1 disease (30.1%),
whereas 86 calves had multiple diseases (2.5%). (D) Mortality rate (%) of female Holstein Friesian calves (n = 3,434) with different categories
of transfer of passive immunity during the first 90 d of life.

different employees (P < 0.01), and day of life for TPI Calves sampled on d 2 had significantly higher % Brix
assessment (P < 0.01) were significantly associated results compared with the remaining sampling days (P
with TS concentration in % Brix (Table 2). Calves from < 0.01; Table 2).
cows in lactation ≥3 had lower % Brix results in serum Average daily weight gain during the first 60 d of life
than calves from primiparous cows (−0.09 ± 0.03% was associated with TPI categories (P < 0.01; Table 1
Brix, P < 0.01) or cows of second lactation (−0.06 ± and 3). Calves with excellent and good TPI status had
0.03% Brix, P = 0.06). We found no statistical differ- ADG of 0.90 ± 0.01 kg/d and 0.92 ± 0.01 kg/d (mean
ence between calves from primiparous cows or cows of ± SE), respectively. The ADG of calves with fair TPI
second lactation (P = 0.38). Dystocia had a signifi- status was 0.89 ± 0.01 kg/d, and calves with poor TPI
cant effect on the TS concentration. Calves requiring had 0.86 ± 0.01 kg/d (Table 1). The ADG of calves
calving assistance had lower % Brix results (score 2: with excellent or good TPI status were respectively
−0.08 ± 0.03% Brix, P = 0.01; score 3: −0.14 ± 0.03% 0.04 ± 0.01 kg/d and 0.06 ± 0.01 kg/d greater that of
Brix, P < 0.01) than calves that were born unassisted. calves with poor TPI (Table 3). Furthermore, the ADG
No statistical difference occurred between calves that of calves with fair TPI was 0.03 ± 0.01 kg/d greater
required calving assistance with 1 or 2 persons (P = that of calves with poor TPI (Table 3). Average daily
0.14). Calves born in the month of April (−0.14 ± weight gain differed in calves with poor TPI compared
0.06% Brix; P = 0.02) had lower % Brix results than with the other categories (fair: P = 0.02; good: P <
calves born in January. The employee providing calving 0.01; excellent: P < 0.01). Additionally, fair (P < 0.01)
assistance and neonatal care significantly affected the and excellent TPI (P = 0.01) differed from good TPI.
TS concentration (Table 2). Furthermore, the day of No statistical difference was found between the TPI
life for TPI assessment influenced TS concentration. categories fair and excellent (P = 0.37).

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 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7049

Figure 2. Kaplan-Meier survival analysis illustrating the association of category of transfer of passive immunity (poor: <8.1% Brix, n = 166;
fair: 8.1–8.8% Brix, n = 1,012; good: 8.9–9.3% Brix, n = 971; excellent: ≥9.4% Brix, n = 1,285) and time to diarrhea (A), time to pneumonia
(B), overall morbidity (C), and mortality (D) during the first 90 d of life. Neonatal diarrhea was defined as visibly loose feces of decreased
consistency. Pneumonia was defined as visibly detectable tachypnea with nasal discharge (serous, mucous, or purulent). Morbidity included the
following diseases: (1) neonatal diarrhea, which was defined as visibly loose feces of decreased consistency, (2) omphalitis, which was defined as
inflammatory signs (redness, swelling, purulent discharge, or painful response to palpation) of the umbilical cord, in addition to fever or lack of
appetence, and (3) pneumonia, which was defined as visibly detectable tachypnea with nasal discharge (serous, mucous, or purulent).

In the generalized linear mixed model TS concen- fixed effect. The greater the % Brix results, the lower
tration in % Brix had no significant association with probability of mortality (Figure 3C).
diarrhea (P = 0.33) and omphalitis (P = 0.59; Table 1).
Pneumonia (P < 0.01), overall morbidity (P < 0.01), DISCUSSION
and mortality (P = 0.03) during the first 90 d of life
were related to TS concentration in % Brix (Table 1). The overall objective of the study was to compare
The estimated probability of developing diarrhea dur- calf health, ADG, and calf mortality considering the
ing the first 90 d of life was estimated including TS proposed categories of TPI by the consensus report of
concentration in % Brix (P = 0.03). Estimates were Lombard et al. (2020) during the preweaning period.
derived from the GENLINMIXED model, including % Furthermore, we looked at calving-related factors and
Brix (P = 0.03) and the quadratic term of % Brix (P their effects on TPI. The main findings of the present
= 0.03) as fixed effects. Calves with TS concentration study were as follows: (1) the TPI status was associated
of 8.0 to 10.5% Brix showed the lowest probability with morbidity and mortality rate; (2) calves with poor
of developing diarrhea (Figure 3A). The probability TPI had greater hazards for diarrhea, pneumonia, or
of developing pneumonia during the first 90 d of life mortality during the weaning period; (3) the greater
was estimated using the GENLINMIXED model and the TS concentration, the lower the probability of de-
including TS concentration in % Brix (P < 0.01) as veloping pneumonia or any disease, or of mortality; and
fixed effect. The greater the % Brix results, the lower (4) calves with excellent, good, and fair TPI status had
the probability of developing pneumonia (Figure 3B). greater ADG.
Probability of mortality during the first 90 d of life The TPI distribution of the farm in the present study
was estimated using the GENLINMIXED model and did not entirely achieve the recommendations of Lom-
including TS concentration in % Brix (P = 0.07) as bard et al. (2020) with a distribution of 4.8% FTPI

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 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7050
Table 2. Associations between parity, calving ease, calving assistance, transfer of passive immunity (TPI)
assessment, birth month, and TS (in % Brix) of female Holstein Friesian calves (n = 3,339)

95% CI
Estimate,
Variable % Brix SE1 Lower bound Upper bound P-value
Intercept 9.660 0.06 9.54 9.77 <0.001
Parity
1 Referent
2 −0.027 0.27 −0.087 0.033 0.376
≥3 −0.087 0.30 −0.140 −0.033 <0.001
Calving ease score2
1 Referent
2 −0.079 0.03 −0.139 −0.019 0.010
3 −0.138 0.03 −0.202 −0.073 <0.001
Birth month
January Referent
February 0.024 0.06 −0.082 0.129 0.663
March −0.091 0.06 −0.203 0.020 0.109
April −0.136 0.06 −0.250 −0.022 0.019
May −0.002 0.06 −0.117 0.112 0.967
June 0.003 0.06 −0.107 0.112 0.964
July 0.049 0.06 −0.064 0.162 0.397
August −0.092 0.06 −0.201 0.017 0.099
September −0.075 0.06 −0.185 0.034 0.177
October −0.005 0.06 −0.113 0.103 0.929
November −0.015 0.06 −0.123 0.093 0.786
December 0.031 0.05 −0.080 0.143 0.581
Calving assistance
Employee 1 Referent
Employee 2 −0.163 0.08 −0.316 −0.010 0.036
Employee 3 0.077 0.05 −0.014 0.169 0.098
Employee 4 −0.107 0.04 −0.180 −0.034 0.004
Employee 5 −0.125 0.04 −0.207 −0.043 0.003
Employee 6 −0.319 0.11 −0.532 −0.107 0.003
Employee 7 −0.016 0.06 −0.137 0.105 0.796
Employee 8 0.038 0.07 −0.095 0.170 0.557
Day of life for TPI assessment
2 Referent
3 −0.277 0.04 −0.363 −0.192 <0.001
4 −0.383 0.04 −0.468 −0.298 <0.001
5 −0.383 0.04 −0.467 −0.298 <0.001
6 −0.556 0.04 −0.639 −0.473 <0.001
7 −0.577 0.04 −0.660 −0.494 <0.001
1
SE = standard error of the estimate.
2
Calving ease scores: 1 = no calving assistance; 2 = calving assistance by 1 person; 3 = calving assistance by
2 persons.

Table 3. Associations of transfer of passive immunity (TPI) in % Brix on ADG of female Holstein Friesian
calves (n = 2,942)

95% CI

Variable Estimate, kg/d SE1 Lower bound Upper bound P-value

Intercept 0.862 0.01 0.84 0.89 <0.001
Category of passive immunity2
Poor TPI Referent
Fair TPI 0.031 0.01 0.005 0.058 0.022
Good TPI 0.057 0.01 0.031 0.084 <0.001
Excellent TPI 0.037 0.01 0.011 0.064 0.005
1
SE = Standard error of the estimate.
2
Category of passive immunity: poor = <8.1% Brix; fair = 8.1–8.8% Brix; good = 8.9–9.3% Brix; excellent =
≥9.4% Brix.

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(<10%), 29.5% fair (20%), 28.3% good (30%) and 37.4%

excellent (40%), respectively (values recommended by
Lombard et al. are in parentheses). One reason for this
might be that the farm management is still focused on
avoiding FTPI, and the new recommendations have not
been implemented into the calf health management.
Raboisson et al. (2016) reported an increased risk
for mortality (2.12 times more likely) associated with
poor TPI, as well as for pneumonia (1.75 times more
likely), diarrhea (1.51 times more likely), and overall
morbidity (1.91 times more likely). These findings are
in accordance with the results of the Cox regression
model of our study, showing greater hazards for calves
with poor TPI regarding mortality (2.47 times more
likely), pneumonia (2.00 times more likely), and over-
all morbidity (1.99 times more likely), and a tendency
for greater hazard of diarrhea (1.57 times more likely)
compared with excellent TPI, respectively. Calves with
excellent TPI compared with the other TPI categories
(fair, good, and poor) had lower probabilities of suffer-
ing from pneumonia (P < 0.01) or overall morbidity (P
< 0.01). Crannell and Abuelo (2023) detected similar
findings: calves with excellent TPI compared with in-
ferior TPI categories had an increased risk of diarrhea
(HR = 1.49), pneumonia (HR = 1.39), and mortality
(HR = 4.29). Nevertheless, Crannell and Abuelo could
not detect a significant difference of pneumonia and
mortality risks between calves with fair or good TPI
compared with excellent TPI. Based on our findings,
we believe the new recommendations of the consensus
report have the potential to reduce morbidity in calves.
In this study, the results from the generalized linear
mixed model indicate that poor TPI was not associ-
ated with diarrhea or omphalitis. This might be due
to the low number of cases of diarrhea (n = 216; 6.3%)
and omphalitis (n = 31; 0.9%) detected in our study.
This contrasts the findings of Crannell and Abuelo
(2023), who detected a proportional increase in the risk
of digestive disorders in calves as the quality of TPI
decreases. Furthermore, a cross-sectional study also
performed in Germany (Dachrodt et al., 2021) found
Figure 3. (A) Estimated probability of diarrhea (%) during the associations, but with less-specific definitions of diar-
first 90 d of life based on TS in serum (% Brix) for female Holstein rhea (i.e., watery, liquid, or soft feces) and omphalitis
Friesian calves (n = 3,434) aged 2 to 7 d. Neonatal diarrhea was de-
fined as visibly loose feces of decreased consistency. Estimates were (i.e., acute and chronic inflammatory cases of the ex-
derived from the GENLINMIXED model, including TS concentration ternal umbilical cord, classified as thickening, swelling,
in % Brix (P = 0.03) and the quadratic term of TS concentration pain, or heat). Dachrodt et al. described much higher
in % Brix (P = 0.03) as fixed effects. (B) Probability of pneumonia
(%) during the first 90 d of life based on TS in concentration (% prevalence rates for diarrhea (18.5%) and omphalitis
Brix) for female Holstein Friesian calves (n = 3,434) aged 2 to 7 d. (20.9%), respectively. In the United States 21.1 ± 2.0%
Pneumonia was defined as visibly detectable tachypnea with nasal (mean ± SE) of preweaning heifer calves have been
discharge (serous, mucous, or purulent). Estimates were derived from
the GENLINMIXED model, including TS concentration in % Brix (P reported to have diarrhea, and 1.7 ± 0.3% (mean ±
< 0.01) as fixed effect. (C) Probability of mortality (%) during the SE) had omphalitis (USDA, 2018), despite the observa-
first 90 d of life based on TS in serum (% Brix) for female Holstein tion that the prevalence of poor TPI had decreased
Friesian calves (n = 3,434) aged 2 to 7 d. Estimates were derived from
the GENLINMIXED model, including TS concentration in % Brix (P from 41% in 1991 (USDA, 1993) to 13% in 2014 (Urie
= 0.07) as fixed effect. et al., 2018b). According to Raboisson et al. (2016), the
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 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7052

risk of diarrhea associated with poor TPI is low. This Raboisson et al. (2016) estimated the total costs per
is related to the high prevalence of diarrheal diseases in dairy calf with poor TPI to be €60 (€10–109). This
calves despite poor TPI, which mathematically limits is not only a severe economic loss but also the high
the value of the risk. disease prevalence represents an animal welfare issue.
In this study 27.9% of the heifer calves (n = 957) were Therefore, the main goal for the dairy industry is to
diagnosed with pneumonia; the overall morbidity was reduce morbidity and mortality during the prewean-
32.6% (n = 1,118), and mortality was 3.1% (n = 107). ing period to achieve high-quality calf management.
The prevalence of pneumonia is in accordance with the A greater number of calves with higher TPI status at
prevalence of respiratory diseases in the United States herd level might help to reduce morbidity and mortal-
of 12.0 ± 1.4% (mean ± SE) in 2014 (USDA, 2018). ity rates.
The high mortality rates caused by diarrhea (56%) and Furthermore, our data show that management factors
respiratory diseases (24%) reported 2014 in the United (i.e., parity, calving ease, calving assistance, and day
States (UDSA, 2018) indicate that it is important to of life for TPI assessment) and environmental factors
reduce calves’ susceptibility to diseases. Our results (birth month) were associated with TS concentration in
support the recommendations of Lombard et al. (2020) % Brix. Calves from multiparous cows (parity ≥3) had
of greater TPI status on a herd level, as the likelihood lower % Brix results (P < 0.01). The reason for this
of developing pneumonia or of mortality decreased remains speculative. As the study farm implemented a
with higher % Brix results. This contrasts the results of standard operating procedure for the first feeding (4 L
Crannell and Abuelo (2023), who found no significant of pasteurized, pooled, colostrum, i.e., ≥22% Brix fed
differences in pneumonia risks between the TPI catego- via esophageal tube feeder), parity could be a subor-
ries fair or good compared with excellent TPI. dinate factor. Therefore, the TS concentration might
Calves with excellent, good, and fair TPI had sig- be an intrinsic characteristic of the calf, such as the
nificant greater ADG compared with calves with poor individual abomasal emptying rate (Mokhber-Dezfooli
TPI in the present study. However, no statistical dif- et al., 2012) or lower calf birth weights of primiparous
ference was detectable between the TPI categories fair cows in relation to the standardized first feeding vol-
and excellent. The reason for this remains speculative. ume.
As described in literature, based on our results, we can Calves experiencing calving assistance had lower TS
confirm a difference in ADG of calves with poor TPI concentration in % Brix (P < 0.01). Vitality of calves
compared with calves with higher % Brix results. This born after dystocia is often compromised, and their at-
is consistent with the findings of Robison et al. (1988) tempts to stand are delayed (Riley et al., 2004; Barrier
and Elsohaby et al. (2019), who observed a significant et al., 2012, 2013). Poor vigor has also been associ-
increase of ADG in dairy heifers with adequate TPI ated with a reduced absorption rate of IgG (Furman-
compared with those with poor. In contrast, Nocek et Fratczak et al., 2011; Barrier et al., 2012) and therefore
al. (1984) found no differences in weight gain of calves a greater risk of poor TPI.
with poor TPI compared with calves with higher serum The % Brix results were associated with the employee
IgG concentrations at 45 d of age. Caldow et al. (1988) providing calving assistance and neonatal care (P <
and Wittum and Perino (1995) observed that animals 0.01). Neonatal calf care and calf rearing requires en-
with poor TPI gained less weight than animals with gagement and motivation. Benchmarking is effective in
adequate TPI but considered this to be an indirect health care, farming, and the commercial industry, to
effect of the increased morbidity observed in animals engage and motivate employees (Jarrar and Zairi, 2001;
with poor TPI. According to Quigley et al. (1995) the Bogetoft, 2012). This offers the possibility to reflect on
differences in ADG are related to the management current practices and identify sources of error (Meade,
conditions of the farm rather than the TPI status of 1994; Anand and Kodali, 2008). Atkinson et al. (2017)
the calves. This finding was confirmed by Crannell and evaluated the effects of benchmarking at the farm level
Abuelo (2023), who also found no difference in ADG on the prevalence of poor TPI and ADG in prewean-
within the 4 TPI categories. Average daily weight gain ing calves in Canada and concluded that benchmarking
is an important measure for assessing calf management motivated producers for management changes with the
quality during the preweaning period (Breen et al., intention to improve performance.
2012). Greater ADG generates more profit for the dairy The day of life for TPI assessment significantly af-
farmer. Soberon and Van Amburgh (2013) showed that fected the % Brix results (P < 0.01). Calves sampled
calves with greater preweaning ADG were 2 times more on d 2 had higher % Brix results compared with the
likely to have greater milk yield in the first lactation remaining sampling days (P < 0.01; range: 0.3–0.6%
(odds ratio = 2.09; P = 0.001), whereas calves suffering Brix). Blood sample collection for TPI assessment is
from poor TPI have lower ADG and increased costs. possible from 24 h after the first colostrum feeding to
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 Sutter et al.: TRANSFER OF PASSIVE IMMUNITY AND FEMALE CALF HEALTH 7053

10 d of age (Wilm et al., 2018; Godden et al., 2019). calves. J. Dairy Sci. 100:3773–3782. https:​/​/​doi​.org/​10​.3168/​jds​
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ACKNOWLEDGMENTS Prevalence of disorders in preweaned dairy calves from 731 dairies
in Germany: A cross-sectional study. J. Dairy Sci. 104:9037–9051.
The study was funded in part by Tiergyn e. V. (Ber- https:​/​/​doi​.org/​10​.3168/​jds​.2021​-20283.
lin, Germany). We gratefully thank the participating Dohoo, I. R., S. W. Martin, and H. Stryhn. 2009. Model-building
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dairy farm for their collaboration and the farm person- 2nd ed. VER Inc.
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any other conflicts of interest. Keefe. 2019. Effect of passive transfer of immunity on growth per-
formance of preweaned dairy calves. Can. J. Vet. Res. 83:90–96.
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