Journal of Equine Veterinary Science 44 (2016) 100–104

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Journal of Equine Veterinary Science

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Original Research

Risk Factors Associated With Failure of Passive Transfer of

Colostral Immunoglobulins in Neonatal Paso Fino Foals
Martha Susana Franco Ayala 1, Olimpo Juan Oliver-Espinosa*
Department of Animal Health, Faculty of Veterinary Medicine and Zootechny, National University of Colombia, Bogota DC, Cundinamarca, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: A year-long prospective cohort study was conducted in Colombian Paso Fino horse farms
Received 24 November 2015 to determine the risk factors associated with total failure of passive transfer. The risk
Received in revised form 6 May 2016 factors associated to management, dam, foaling and foal were correlated with failure of
Accepted 9 May 2016
passive transfer. Foal’s IgG levels were measured using an ELISA test at 24 hours of life; a
Available online 26 May 2016
test agreement to predict failure of passive transfer between the ELISA test and total
plasma proteins was evaluated. X2 test and multinomial regression were also performed.
Keywords:
Ó 2016 Elsevier Inc. All rights reserved.
Colostrum
ELISA test
Mares
Total plasma proteins

1. Introduction (TFPT) is commonly defined by several authors as serum

Foals are immunocompetent at birth; however, they are
hypogammaglobulinemic, and their autologous immuno-
globulins (Igs) are not significantly detectable in serum
until approximately 2 months of age [1]. The initial hu-
moral immunity is provided by Igs passively acquired via
colostrum intake within the first 24 hours of life [2].
Different factors may negatively influence the neonatal
absorption of colostral Igs, often resulting in failure of
passive transfer (FPT) of Igs [3,4].
Colostrum consumption by normal foals starts within
2 hours after birth, and maternal antibodies are detected
within 4 to 6 hours in neonate foal’s serum [5]. Absorption
of macromolecules including Igs is done by pinocytosis.
This absorption in neonatal foals is more efficient in the
first 3 to 6 hours of life, and it is minimal by 20 hours [2,6].
Despite great controversy, total failure of passive transfer
* Corresponding author at: Olimpo Juan Oliver-Espinosa, Department
of Animal Health, Faculty of Veterinary Medicine and Zootechny, National
University of Colombia, Carrera 45 # 26-85 Edificio Uriel Gutierrez,
Bogota DC, Cundinamarca, Colombia.
E-mail address: ojolivere@unal.edu.co (O.J. Oliver-Espinosa).
1
Present address: Carrera 2 este 18-75 Chia, Cundinamarca, Colombia.
immunoglobulin G (IgG) concentration of <4 g/L measured
at 24 hours after birth, partial failure of passive transfer
(PFPT) is defined when serum IgG concentrations are be-
tween 4 and 8 g/L, and adequate IgG absorption is
considered above 8 g/L [3,7,8].
The reported incidence of FPT in foals ranges between
2.9% and 25% [3,7,9] and PFPT incidence to 18.6% [10] in
different studies. Failure of passive transfer is generally
regarded as one of the most important risk factors (RFs) for
diseases and death in neonatal foals [11–13].
Various factors associated with FTP have been
described, including poor colostrum quality of the dam and
reduced colostrum intake by foal or disorders affecting
intestinal absorption in the foal [14–16]. Colostrum quality
is determined by mother’s age, breed [10], nutritional sta-
tus, premature lactation, and premature delivery and by
low colostrum production observed in stressed mares,
mares with mastitis or structural damage to the udder
[14,16]. A major factor that commonly affects colostrum
quality in mares is fescue-associated toxicity [17]. Colos-
trum consumption of the foal may be affected by the ability
to stand up and suckle as soon as possible after birth. This
can be observed in weak foals with musculoskeletal

0737-0806/$ – see front matter Ó 2016 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.jevs.2016.05.006
 M.S. Franco Ayala, O.J. Oliver-Espinosa / Journal of Equine Veterinary Science 44 (2016) 100–104
abnormalities and in foals with maladjustment syndrome
[3,15,16]. Intestinal colostrum absorption may also be
affected by prematurity reducing absorption of macro-
molecules by an underdeveloped intestinal mucosa.
Recently, this has been associated with the excessive
release of endogenous corticosteroids and with foals
suffering from comorbidities such as maladjustment syn-
drome, prematurity, and sepsis [3].
Several qualitative or quantitative tests have been used
to determine plasma IgG levels in foals. The most accurate
quantitative test to date is the simple radial immunodif-
fusion (SRID), considered as the gold standard, but its use is
limited because the results are delayed 72 hours [18];
among the qualitative tests are: latex agglutination test,
clotting glutaraldehyde, and zinc turbidity test [19]. A new
automated turbidimetric immunoassay test when
compared with SRID as gold standard has shown a high
sensitivity of 92% and low specificity of 63% for detecting
FPT [20]. Recently, the enzyme-linked immunosorbent
assay (ELISA) test has been used as a semiquantitative
method for the determination of IgG [21]. This is a quick
and easy field technique, which has been shown in several
studies to have both a high sensitivity (80%, 89%, and 81%)
and high specificity (90%, 95%, and 94.7%) [22–24]. The
ELISA test has been designed to detect the presence of IgG
using polyclonal antibodies against equine IgG. To perform
the test, a sample of anticoagulated blood is used. Anti-IgG
antibodies capture the equine IgG in the sample. The
enzyme-conjugated polyclonal antibodies are added to
bind the captured equine IgG forming an antibody-IgG-
antibody sandwich [25].
To indirectly determine the passive absorption of Igs,
the total plasma protein (TPP) concentration has been used.
Koterba et al [15] established that TPP < 45 g/L indicated
TFPT, whereas TPP > 55 g/L was associated with optimal
absorption of Igs. Its diagnostic utility has been evaluated in
some studies in which it showed a sensitivity of 94% and a
specificity of 83%. In addition, Hurcombe et al [26] found
that serum proteins have a greater sensitivity than TPP to
predict FTP and they established a cutoff point of serum
protein concentration of
45 g/L for TFPT and 60 g/L for
optimal passive transfer; they also consider that the TPP is
an unreliable predictor of TFPT in contrast to other authors.
The main objectives of this study were to determine the
RFs associated with the presentation of TFPT in a yearlong
prospective study and to determine the agreement be-
tween IgG ELISA Test and TPP concentrations for diagnosing
TFPT and PFPT.
2. Materials and Methods
A prospective cohort study was conducted using a
purposive sampling technique to select the Paso Fino horse
farms for the study. The farms included in the study were
those whose owners accepted to participate in the study
and were located in the Savannah of Bogotá. A survey was
applied to the staff personnel at the farms using multiple
choice questions about management, pasture, and foaling
sites and also questions with dichotomous answers such
as: whether foaling occurred at night or during the day.
Initially, the surveys on management practices for each
101
farm were implemented at the time farms were selected for
the study. An individual survey for each mare and foal was
applied when the foals were born. Each foal was examined
within the first 72 hours of life by one of the researchers
and the farm staff personnel. Venous blood samples were
drawn between 24 and 72 hours of life to measure foals’ IgG
concentration. A daily monitoring system for each foal was
implemented, and one researcher visited the farm weekly
until foals were 30 days old.
2.1. Risk Factors
A survey that contemplated the major RFs was imple-
mented, and the factors were classified according to being
either associated to the farm, dam, foaling, or the foal itself.
The size of the farm, particulars of feed supplementation of
the pregnant mare, foaling site, and water source were
recorded as potential farm RFs.
Risk factors hypothesized to be associated to the mare
were age, body condition, parity, whether it was a brood
mare or a recipient and disease during the pregnancy.
The RFs at foaling: time of foaling (day/night), whether
assistance for delivery was needed, time of expulsion of the
placenta, and its appearance; all potential RFs and variables
are summarized in Table 1.
Potential foal RFs included: an assessment report by the
owner or farm staff personnel on whether the foal was
normal at birth on the presence of several signs such as:
weakness, inability to stand up, absence of suckling reflex
and depression; report of time to stand up (<1 hours or
>1 hour) [11] and time to consume colostrum (<6 hours or
>6 hours) [16]; weight at birth (kg); clinical examination
within the first 24 to 72 hours of life; determination of
immaturity (silky skin coat, lax flexor tendons, small size,
pliant ears, gestation length [>320 days or < 320 days]); IgG
levels measured using an ELISA test (IDEXX SNAP Foal IgG
Test Kit; IDEXX Laboratories, Inc) done at the farm and TPP
measurement by refractometry (Clinical usage and Veteri-
nary Refractometer RHC-200ATC; WMicro) carried out at
the Veterinary Clinical Pathology Laboratory of the National
University of Colombia at 24 to 72 hours of life (see Table 1).
In this study, FPT, TFPT, PFPT, and adequate absorption of
maternal Ig (no FPT) were defined as foals with serum IgG
concentrations at 24 to 72 hours of life of <8 g/L, <4 g/L,
4 g/L to 8 g/L, and >8 g/L, respectively [9].
Whole blood was used to run the ELISA test according to
manufacturer’s guidelines. The comparisons between the
ELISA test results and TPP were done at IgG concentration
ranges of: <4 g/L (TFPT), 4 to 8 g/L (PFPT), or >8 g/L (not
FPT) [9].
2.2. Statistical Analysis
Sample size calculation was performed using a signifi-
cance of 95% and a power of 80%. The calculated sample size
was 249 foals, but only 192 foals were born and available
for the study in the 35 participating farms during the study
period [27]. The chi-square test (P < .05) was used to
determine significant association between the potential
RFs and TFPT/PFPT. A univariate relative risk (RR) was
calculated for those potential RFs that were determined
102 M.S. Franco Ayala, O.J. Oliver-Espinosa / Journal of Equine Veterinary Science 44 (2016) 100–104

Table 1 took less than an hour to get up, and the first colostrum
The chi-square test to determine significant statistical association be- intake took place within the first 6 hours of life in 93.6% (n
tween potential risk factors and TFPT (P < .05).
¼ 177) of the cases. A total of 180 (95.24%) neonates suckled
Risk Factor Variable X2 TFPT directly from the dam, 9 (4.76%) foals received colostrum
Farm size Large, medium, small 0.58 from the dam by bottle-feeding. Two foals consumed
Presence of other animal Yes/no 0.81 colostrum from an equine colostrum bank, in one using
species on the farm
bottle-feeding and in the other by stomach tubing, and a
Water source Aqueduct, well, broken 0.28
Vaccination on the farm Yes/no 0.56 third foal received cow’s milk; all these three foals were
Deworming program on the farm Yes/no 0.95 included in the study.
Waste disposal Direct paddocks, 0.45 Using the ELISA IgG Test in neonatal blood, an FPT
compost, other incidence of 22.74% (n ¼ 43), a TFPT incidence of 14.81% (n
Delivery site Pasture, stable 0.039*
Mother’s age, y <5, 6–10, 10–15, >15 0.88
¼ 28), and a PFPT incidence of 7.93% (n ¼ 15) were
Number of births of mother Multiparous or 0.031* observed. Adequate absorption of immunoglobulin was
primipara determined in 77.26% of the foals.
Pregnancy type Brood mare or receptor 0.19
Maternal body condition score 1–6 0.51
Accommodation mother Pasture or stable 0.024* 3.1. Evaluation of Risk Factors Associated With the TFPT
in pregnancy
Mineral salt administration Yes/no 0.87
Determination of the RRs indicated that foals born in
to the dam
Concentrate administration Yes/no 0.089 stables, foals that the farm staff personnel’s report indi-
to the dam cated abnormality, the ones that took longer than 1 hour to
Stay on the farm before <1, 1-6, >6 0.56 stand up, the foals that consumed colostrum after 6 hours
parturition, mo postpartum, and the ones that were deemed immature had
Pregnancy history Normal or abnormal 0.498
an increased risk to develop TFPT (IgG
4 g/L); however,
Signs of placentitis Yes/no 0.65
Gestation period, d <320, 320–340, >340 0.18 foals born to multiparous mares had a lower RR to have
Time of birth Day or night 0.154 TFPT (see Table 2).
Assisted parturition Yes/no 0.94 These factors were analyzed using a multinomial
Retained placenta Yes/no 0.85
regression using a “stepwise” approach. The final model
Placental abnormalities Yes/no 0.56
Foal appreciation by farm Normal or abnormal 0.041*
included: time to stand up and type of housing manage-
staff personnel ment. An increased risk of TFPT was observed in foals that
Gender Male or female 0.88 took longer than 6 hours postpartum to consume colos-
Time to stand up after birth, hr <1 or >1 0.00* trum (odds ratio: 5.39; confidence interval [CI] 1.48–19.58),
Colostrum source Mother, colostrum 0.2
whereas foals from mares that were born on pasture had a
bank, others
Time to first colostrum <6 or >6 0.00* lower risk of developing TFPT when compared with foals
intake (<6 hr, >6 hr) from mares housed in stables (odds ratio: 0.23; CI 0.086–
Navel disinfection Yes/no 0.17 0.62; see Table 3).
Numbers of navel disinfections 1 time, 2–5 times, 0.94
>5 times
Product used to disinfect the navel Iodine, chlorhexidine, 0.97 3.2. Degree of Agreement Between the ELISA Test and TPP for
others Diagnosis of TFPT
Foal weight. kg <20, 20–30, >30 0.8
Dysmaturity Yes/no 0.035*
Prematurity Yes/no 0.23 The kappa statistic showed a 61.8% agreement between
TPP concentration and the ELISA test for complete absorp-
Abbreviation: TFPT, total failure of passive transfer.
* Statistically significative association.
tion of Igs, whereas for TFPT, the agreement was only 40.33%.

4. Discussion
statistically significantly associated (P < .05). All these po-
tential factors that were found to be statistically associated Given that determining IgG absorption from colostrum
(P < .05) were evaluated in a multivariate analysis, using a in foals is of paramount importance in preventing early
stepwise trial approach and interaction tests before being diseases in neonatal foals, identifying the RFs associated
included in a multinomial regression model [28,29]. This
analysis was performed using SAS statistical software (SAS
9.2; SAS Institute Inc, Cary, NC). The degree of agreement Table 2
Relative risk values of factors that were determined to be significantly
between the ELISA test and TPP for TFPT, and no FPT was associated with TFPT by the chi-square test (P < .05).
determined using the Kappa statistic (K) [30].
Risk Factors X2 RR Confidence Interval
Stayed on stall 0.024 2.56 1.3–7.89
3. Results
Multiparous mares 0.031 0.41 0.21–0.79
Findings negative birth 0.041 2.1 1.07–4.2
A total of 192 neonatal foals were followed in this study; Time to stand up >1 hr 0.000 3.68 1.85–7.31
however, three foals died before 24 hours of life, preventing Colostrum intake >6 hr 0.02 2.69 1.22–5.9
determination of Ig absorption in them. Therefore, 189 foals Dysmature foal 0.035 2.88 1.4–5.8

were used in the study. It was found that 178 (94.17%) foals Abbreviations: RR, relative risk; TFPT, total failure of passive transfer.
 M.S. Franco Ayala, O.J. Oliver-Espinosa / Journal of Equine Veterinary Science 44 (2016) 100–104
Table 3
Results of multinomial regression for TFPT in Paso Fino foals in the first
month of life.
Risk Factor Serum IgG Odds Ratio Confidence
Concentration Interval
Intercept (B1) 0.38
Time to stand up >1 hr
4 g/L 5.39 1.48–19.58
Kept on pasture versus stall
4 g/L 0.23 0.086–0.62
Abbreviations: RR, relative risk; TFPT, total failure of passive transfer.
with FPT in Paso Fino foals will allow establishing protocols
for diagnosis, prevention, and control of FPT in this specific
breed [31,32].
Total lack of colostrum intake in newborn foals has been
associated with neonatal septicemia [31,33] and early
death in foals [11]. The method of colostrum administration
has also been associated with increased systemic disease
with diarrhea in foals [12]. This RF was evaluated, but in
this study, no association was found with TFPT.
Failure of passive transfer depends on multiple RFs
associated with parturition. Morley and Townsend [34]
found that foals born during mild dystocia deliveries have
increased risk of TFPT, whereas those that suffered severe
complications during birth have a higher risk to develop
TFPT; however, despite that 4.1% of all deliveries required
assistance in the present study, no association with TFPT
was found. The factors determined to be associated with
FPT were foals that took longer than an hour to stand up
and consumed colostrum for the first time after 6 hours of
life. These findings are related to physiological character-
istics that demand that a normal newborn foal should stand
in less than an hour to be able to consume colostrum
adequately [15], a delay in standing up could be an indi-
cation of weakness that can hinder colostrum intake and
may lead to FPT [3,34].
Foals born to multiparous mares showed lower risk of
TFPT (RR 0.41; CI 0.21–0.79); this is in contrast to the study
by Morris et al (1985) [10] who found that neither the
mare’s age nor the number of foalings are related to
colostrum quality and to the study in Standardbred foal
that showed that maiden (primiparous) mares had less FPT
in their foals, but, the association was not statistically sig-
nificant [35]. As for this association in the present study, no
explanation could be hypothesized despite that age and
parity could make biological sense to be important in the
mare’s mothering abilities, udder development or colos-
trum quality.
Dysmature and premature foals have been shown to be
more prone to develop disease during the neonatal period
and to suffer early death [12,34] compared with full-term
foals. In this study, dysmature neonatal foals showed an
increased risk of having a higher risk of FPT. This increased
RR for TFPT in dysmature foals was more than two times
compared with full-term foals. Dysmature foals tend to
show marked skeletal muscle abnormalities that may delay
getting up and to suckle the first colostrum [36]; they may
also have alterations in the gastrointestinal tract, poten-
tially predisposing them to FTP, to gastrointestinal disor-
ders and/or infections in the neonatal period [3].
The types of housing facilities used for the mare were
associated with TFPT. Mares kept on pasture were less
103
likely to have foals with TFPT. Neonatal foals born to mare
that foaled in stables have also been associated previously
with a higher predisposition to get sick early in life [37]. A
tentative explanation for this finding is that grazing mares
undergo lower stress levels, and it also influences positively
its mothering skills.
The ELISA test is a rapid test for field use, and it has been
proven to have a high sensitivity and specificity in diag-
nosing FPT [1,22,23]. It is a reliable tool to diagnose FPT in
the field [23]. A comparison between this ELISA test
method and the measurement of TPP using a kappa statistic
showed a low level of agreement for prediction of TFPT (K:
40.3%) and a moderate agreement when optimal absorp-
tion of IgG was measured (K: 60.8%). This suggests that
based on the high sensitivity and specificity of the ELISA
test, the measurement of TPP is a relative good predictor of
total IgG absorption but is not reliable when evaluating
TFPT.
Total plasma protein has been overestimated as good
predictive test for diagnosis of FPT. The overestimation
could be caused by the measurement the plasma total
solids, which can be affected by increases in cholesterol,
lipoproteins and glucose, and other factors such as dehy-
dration and systemic illness [3,26]. Interestingly, a study
determined that total serum protein concentration, instead
of TPP, have a sensitivity of 94.11% and a specificity of 83.3%
when compared with the single radial immunodiffusion
[25].
This study has several limitations that include the fact
that it is a purposive sampling study; it had limited number
of farms and of born foals. All these aspects may limit its
external validity. By being a purposive sampling study
based on the owner’s willingness to participate, it may have
biased farm selection toward the ones that are more
receptive to incorporate new technological management
tools and had better management resulting in a sample
that does not represent the whole spectrum of Paso Fino
horse farms in the area of study. Another limitation was the
number of foals included in the study that did not amount
to the calculated sample size although the foals in the study
were all the foals born at the farms during the study period.
These events can limit the conclusions pertaining to the
Paso Fino foal population drawn from this study. In spite of
these limitations, this initial study on Paso Fino Foals can
set the basis for further studies that could lead to clarify all
the factors involved in FPT in this breed.
5. Conclusions
To the authors’ knowledge, this is the first study to
determine the incidence to FPT in Paso Fino foals along
with determination of RFs associated with it. The overall
incidence of FPT on the studied farms was 22.74%, which is
lower compared with that of other studies in other breeds.
Paso Fino foals taking over an hour to stand up have a
higher risk of TFPT, whereas Paso Fino foals born to dams
on pasture had lower risk of showing TFPT in comparison to
ones born to stabled mares. Total plasma protein had a
moderate agreement level with the ELISA test when
measuring adequate Ig absorption in Paso Fino foals, but,
the agreement was very low when determining TFPT.
104 M.S. Franco Ayala, O.J. Oliver-Espinosa / Journal of Equine Veterinary Science 44 (2016) 100–104
6. Ethics and Biosafety Committee
The Ethics Committee for Animal Use at the Faculty of
Veterinary Medicine and Zootechny, the National Univer-
sity of Colombia approved this study. This approval was
done under law 84/89 and resolution 8430/93 of the Re-
public of Colombia.
Acknowledgments
The authors disclose that they have no conflicts of
interest.
This article represents a portion of thesis submitted by
Dr Franco to the Graduate College of the Faculty of Veteri-
nary Medicine and Zootechny, National University of
Colombia as partial fulfillment of the requirements for a
Master of Science Degree.
This work was supported by the Research unit, Faculty
of Veterinary Medicine and Zootechny, National University
of Colombia (Grant number: 16966).
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