PEDIATRICS Vol. 87 No. 4 April 1991 439
Human
Breast
Milk Contains
Bovine
lgG.
Relationship
to Infant
Colic?
Patrick
S.
Clyne,
MD, and
Anthony
Kulczycki,
Jr, MD
From the Washington University School of Medicine, St Louis, Missouri
ABSTRACT. Previous studies have suggested that an unidentified cow’s milk protein, other than 9-lactoglob-ulin and casein, might play a pathogenetic role in infant colic. Therefore, a radioimmunoassay was used to analyze human breast milk and infant formula samples for the
presence of bovine IgG. Milk samples from 88 of the 97
mothers tested contained greater than 0.1 sg/mL of
bo-vine IgG. In a study group of 59 mothers with infants in the colic-prone 2- to 17-week age group, the 29 mothers of colicky infants had higher levels of bovine IgG in their breast milk (median 0.42 zg/mL) than the 30 mothers of noncolicky infants (median 0.32 g/mL) (P < .02). The highest concentrations of bovine IgG observed in human milk were 8.5 and 8.2 g/mL. Most cow’s milk-based infant formulas contained 0.6 to 6.4 ig/mL of bovine
IgG, a concentration comparable with levels found in many human milk samples. The results suggest that appreciable quantities of bovine IgG are commonly pres-ent in human milk, that significantly higher levels are
present in milk from mothers of colicky infants, and that bovine IgG may possibly be involved in the pathogenesis of infant colic. Pediatrics 199i;87:439-444; bovine
im-munoglobulin G, infant colic, human milk, infant formula, cow’s milk proteins.
Infant colic is a disorder that involves
intermit-tent unexplained excessive crying, usually
occur-ring in the first 4 months of life.’ The prevalence of colic is approximately 20% in both formula-fed
infants
and
exclusively breast-fed infants.3’4 Severalstudies suggest that a cow’s milk protein in diets of
formula-fed infants may play a pathogenetic role in colic.1’2’4 To explain why colic affects infants who are exclusively breast-fed, it has been hypothesized
Received for publication Feb 5, 1990; accepted Apr 17, 1990.
Presented, in part, at the American Pediatric Society, Society
for Pediatric Research meeting, Washington, DC, May 1989.
Reprint requests to (A.K.) Division of Allergy and Immunology,
Washington University School of Medicine, 660 S Euclid, Box
8122, St Louis, MO 63110.
PEDIATRICS (ISSN 0031 4005). Copyright © 1991 by the
American Academy of Pediatrics.
that a cow’s milk protein responsible for colic might be absorbed from dietary sources by mothers and transferred in human breast milk.7’8 In previous
tests of this hypothesis,7’8 mothers of 85 nursing
infants with colic were given milk-free diets for
approximately a week. Colic disappeared in 48 of
the breast-fed infants and recurred in 35 of the 48
infants after reintroduction of cow’s milk into the
maternal diet.7’8 Ten mothers were further tested in double-blind crossover fashion; colic developed
in nine of their nursing infants after maternal
ingestion of capsules containing cow’s whey
pro-teins.8
Apparently the search for the responsible protein halted after findings of only minimal amounts of bovine 3-lactoglobu1in (5 to 33 ng/mL,#{176}i to 20 ng/ mL,’#{176}and 0.i to 6.4 ng/mL”2) and casein (i.5 to
i7 ng/mL’#{176}) in human milk. Such concentrations
appear comparable with levels of other dietary an-tigens in human milk” but insignificant relative to
the milligram
per
milliliter levels of casein and lactoglobulin in infant formula. However, humanmilk has not previously been tested for the presence of bovine IgG, even though cow’s milk contains 0.7 mg/mL of bovine
IgG’3
and bovine IgG has beenshown to be antigenic in humans.’4”5
In this study we detected bovine IgG in uS of
i24 human breast milk samples by using a
solid-phase radioimmunoassay (RIA). Levels of bovine
IgG in some human milk samples were comparable with levels in several cow’s milk infant formulas. Levels of bovine IgG were significantly higher in breast milk fed to infants with colic than in breast milk of mothers without colicky infants. Implica-tions of these findings are considered.
METHODS
Study Population
and Human
Milk
Healthy breast-fed infants and their mothers
were recruited through outpatient private practices
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and the La Leche League. Colic was assessed ac-cording to these guidelines: prolonged paroxysms of vigorous crying in healthy infants with normal
physical examination results, with excessive crying
occurring at least 4 days/week for at least a week.
We mainly recruited and studied infants with colic and infants in the colic-prone age range of 2 to i7 weeks3 and excluded borderline cases. All infants were assessed for the presence of colic during their
first 10 weeks and had been exclusively breast-fed during that period. Mothers collected samples of
breast milk into sterile tubes by using either breast
pumping or manual expression. Samples were
im-mediately refrigerated and assayed promptly (47% within 24 hours, 75% within 72 hours) or frozen.
Purification
of Bovine
IgG, Rabbit Antiserum
to
Bovine
IgG Fc Fragments
Bovine IgG was purified from raw cow’s milk as
described previously.’6 Bovine milk IgG was di-gested with i% mercuripapain for 3 hours at 37#{176}C in 0.Oi mol/L sodium phosphate-0.i5 mol/L NaCl pH 7.4 buffer, (phosphate-buffered saline),
contain-ing 2 mmol/L EDTA and iO mmol/L L-cysteine.’7
Bovine Fc fragments were isolated by DE-52 chro-matography,’7 eluting in 7 mmol/L phosphate-0.i mol/L NaCl pH 7.7 buffer, and were free of intact
IgG and Fab fragments on immunoelectrophoretic analysis.
A 3-month-old New Zealand White rabbit was immunized intraperitoneally with 0.5 mg of bovine milk IgG Fc fragments in complete Freund’s adju-vant (Difco, Detroit, MI). Simultaneously, toler-ance to human IgG was induced by intravenous injection of 2.5 mg of half human IgG (chromato-graphically purified, Cappel Laboratories, West Chester, PA), and 2.5 mg of human IgG purified from a normal donor’s serum. The rabbit was boosted every 2 weeks with 0.5 mg of bovine Fc
fragments in incomplete Freund’s adjuvant
(GIBCO, Grand Island, NY), equally divided
be-tween intraperitoneal and subcutaneous injections.
Antiserum was obtained 2 weeks after the fifth
boosting immunization. This antiserum was shown
by immunoelectrophoresis to bind bovine IgG and
its
Fc fragments but not bovine serum IgA nor human IgG. The IgG fraction of the antiserum, obtained by precipitation with 40% saturated (NH4)2S04, was used for the RIA.Solid-Phase
Radioimmunoassay
for Bovine
IgG
Polystyrene tubes (i3 x iOO mm, Becton
Dick-inson, Oxnard, CA) were coated with i mL of the
IgG fraction (i:3000 dilution) of the rabbit
anti-serum to bovine milk IgG Fc fragments in 0.Oi mol/
L Tris buffer (pH 9.0) by incubation overnight at
37#{176}Cand then 4 hours at 4#{176}C.To minimize
non-specific binding, 0.i mL of the IgG fraction (i:34 dilution in the same buffer) of normal rabbit serum
was added and the incubation sequence was
re-peated. Tube contents were aspirated and tubes were stored in i.0 mL of 0.02% sodium azide at 4#{176}C
until assay. Purified bovine milk IgG was labeled
with 1251 by the chloramine T method’8 with 3.7 x
io
Bq (i mCi) carrier-free 1251 and iOO zg ofchlor-amine T per
400
ig of protein in 0.5 mL yieldingspecific activities of approximately i.5 x i06 cpm/
sg.
The RIA was performed in triplicate in phos-phate-buffered saline buffer containing 0.02% so-dium azide and 0.i% human serum albumin (essen-tially globulin-free, Sigma Chemical Co, St Louis, MO). Assay mixtures were added to the antiserum-coated polystyrene tubes in a 0#{176}Cbath. In order of addition, assay mixtures consisted of buffer (0.7 mL), appropriately diluted samples (0.i mL) or
purified bovine IgG standards (2 to i000 ng in 0.i
mL), and 50 000 cpm of ‘25I-labeled bovine milk
IgG
(0.1
mL). After vortex mixing, tubes werecounted and incubated overnight at 37#{176}C.Tube
contents were aspirated and tubes were washed once and recounted.
The limit of sensitivity, 0.05 to 0.i ig/mL of
sample, was determined by the linear range (probits
graph) of the standard curves. Further validation
of the assay was performed by measurement of
multiple sample dilutions, eg, legend to Figure. Ad-ditions of samples or standards to known samples demonstrated that constituents of human milk and diluted formula did not significantly affect the
as-say results. As an internal control, pasteurized cow’s milk samples (measured in i:iOO and i:200
dilutions) contained ‘-500 &g/mL of bovine IgG, comparable with levels in raw cow’s milk.” Also, this assay did not cross-react with bovine casein, 3-lactoglobulin, or a-lactalbumin (all from Sigma Chemical) at iO g/mL, nor with 3 mg/mL of human secretory IgA (Accurate Chem Corp, West-bury, NY), iO mg/mL of human IgG (Cappel), or
iO mg/mL of human serum albumin. (In testing for
human serum albumin cross-reactivity 0.i% oval-bumin was substituted as carrier protein in the
buffer.) Intraassay coefficients of variation ranged
from 3% to 6%; interassay coefficients of variation ranged from 6% to 20%.
Statistical Analysis
In the statistical analysis, mothers are the unit
of comparison of the groups, eg, when multiple milk
I 0 z 0 I-. z uJ I-) z
9
‘-I Ui z > 0 I II. I SI II. 0 --6 0 0 0,TABLE 1. Comparison of Bovine IgG Concentrations in Fresh Human Breast Milk Samples and Their Skim Fractions*
ARTICLES 441
an individual mother, the mean value is used as a
single data point. The concentrations of both
groups in the Figure (and log transformation of one
group) do not fit a gaussian distribution. Therefore, a nonparametric statistical method, the analysis of
variance, was performed by using the general linear models procedure from the SAS computer package
(SAS Institute, Cary, NC).
RESULTS
One hundred twenty-four human milk samples
from 97 mothers were analyzed for bovine
IgG
by solid-phase RIA. One hundred fifteen samples from 88 mothers contained greater than 0.i tg/mL ofbovine IgG or its antigenically detectable
frag-ments. In the study group of 59 mothers (80 breast milk samples) with infants in the colic-prone 2- to i7-week age range, samples from 56 mothers (77 milk samples) contained measurable levels of
bo-vine IgG (greater than 0.i g/mL). All 29 mothers
of infants with colic provided samples containing greater than 0.22 g/mL of bovine IgG (Figure). In contrast, breast milk from 8 of 30 mothers of non-colicky infants contained less than 0.22 jzg/mL of bovine IgG, ie, no exclusively breast-fed infant
de-veloped colic if maternal milk contained less than
0.22 g/mL during the colic-prone period. The con-centrations of bovine IgG in milk samples
associ-ated with infant colic (median 0.42 sg/mL) are significantly higher than concentrations in samples associated with absence of colic (median 0.32 g/
mL) (P ‘= .0i54). There were no significant differ-ences in age or source of referral between the
groups.
Bovine IgG levels were also measured in milk
samples from additional mothers whose children
were either younger than 2 weeks of age (i5
sam-ples) or older than i7 weeks of age (24 samples).
The highest bovine IgG concentrations, 8.5 and 8.2 g/mL, were measured in breast milk from mothers
of infants younger than 2 weeks old, one who later
developed severe colic and one without colic,
re-spectively. Overall, 7 milk samples from four
moth-ers contained greater than i tg/mL of bovine IgG.
Fresh milk samples from seven mothers were
centrifuged at 30 000 X g at 4#{176}Cand cream, skim,
and cellular fractions were separated. Bovine IgG
concentrations of skim fractions paralleled levels of whole breast milk measured in the same assay
(Table i). In several experiments cream and cellular
fractions were analyzed and only a small fraction (usually <iO%) of the bovine IgG content of fresh human milk was detected in the cream supernatant or the cellular pellet. The bovine IgG measured in
skim fractions of two samples was not precipitated
COLIC NO COLIC
Figure. Concentrations of bovine IgG in human milk and presence of colic in infants between the ages of 2 and
17 weeks. Milk samples were obtained from 29 mothers
(38 samples) with colicky infants (#{149})and from 30
moth-ers (42 samples) with noncolicky infants (0). These data
represent single samples from 43 mothers and the average
of samples obtained on different days from 16 mothers. Of the 80 samples, 21 were measured in at least two independent assays and average values are presented. The three lowest values were undetectable at, and are
plotted at, 0.05 and 0.1 ig/mL. Dashed lines
(- - -)
indicate median values. A twofold dilution of the sample
with the highest bovine IgG level (4.6 .tg/mL) resulted in the expected concentration (2.2 tg/mL).
Individual Milk, tg/mL Skim, ig/mL % of Bovine
IgG in Skim
1 0.i69 0.ii4 67
2 0.230 0.132 57
3 <0.05 <0.05 ...
4 2.24 1.5 67
5 0.272 0.125 46
6 0.232 <0.10 <43
7a 0.240 0.112 47
Th 0.236 0.131 56
7c 0.174 0.i28 74
* Each value represents the average of triplicate
deter-minations in a single assay in which both whole milk and skim fractions are compared. Aliquots of freshly obtained
samples were centrifuged at 30 000 X g for 30 minutes at
4#{176}C.After removal of solid cream layers with cold spa-tulas, skim fractions were aspirated from the cellular
pellets. Three samples of breast milk were obtained over
a period of 40 h from donor 7.
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after acidification to pH 4.5 (unlike casein) but was
85% to 96% precipitable in 50% saturated
ammo-nium sulfate (as expected for an immunoglobulin). Multiple samples from individual mothers had little variability in bovine IgG levels, eg, three milk
and skim samples collected within a 40-hour period (donor 7 in Table i) had coefficients of variability
of i7% and 8%, respectively. Also, bovine IgG levels from nine refrigerated samples assayed before and
after freezing matched closely (median difference,
2%).
Commercially available infant formulas were
as-sessed for bovine IgG concentration by solid-phase
RIA (Table 2). As expected, soy-based and hydro-lyzed casein-based formulas had no detectable bo-vine IgG (Table 2 legend). All cow’s milk-based formulas contained detectable levels of bovine IgG. Milk-based formulas contain i5 mg/mL of protein, i4%’#{176}to 60% of which is whey protein. Inasmuch as IgG accounts for ....J/7 ofwhey protein,’9 one might
anticipate a bovine IgG level of 0.3-i.3 mg/mL. However, heat lability of bovine IgG2#{176}may account
for the lower and variable levels observed. In
gen-era!, milk-based formulas prepared from liquid con-centrates contained the lowest levels of bovine IgG (0.6-2.5 sg/mL). The highest levels of bovine IgG
were found in three different lots ofa whey-predom-inant powdered formula from one company. Com-parison of human milk with cow’s milk-based
for-mula preparations surprisingly shows that 20
hu-man milk samples had higher bovine
IgG
levelsthan one milk-based formula.
DISCUSSION
In this study bovine IgG was detected in
concen-trations from 0.i to 8.5 sg/mL in most human milk samples. Both the nature of this protein and its
levels are remarkable. Bovine
IgG
is a uniquean-tigen because it can bind to Fc receptors of human antigen-presenting cells,’6’2’ it can (in these
concen-trations) modulate antibody secretion by human B cells in vitro,2’ and it has a prolonged half-life. The
concentrations of bovine IgG in human milk are
much greater than other dietary antigens previously
reported (only nanogram per milliliter
concentra-tions),9’2 are appreciable relative to reported con-centrations of human
IgG
in milk (averaging 29 ig/mL),22 and are comparable with the serum levels of immune complexes present in various disease
states.23 The microgram per milliliter levels of
bo-vine IgG in some human milk samples suggest that maternally ingested bovine IgG may be relatively
resistant to proteolysis or selectively absorbed or
transported. A precedent for transport is that
bo-vine and human IgG bind equally well to bovine mammary gland tissue.24
Although individual mothers tend to have repro-ducible levels of bovine IgG in repeated samples of their breast milk, a marked variability of bovine IgG concentrations was observed among different
mothers. The sources of population variability are not known but might be related to dietary intake
of dairy products, presence of antibodies to bovine IgG, completeness of digestion of bovine IgG, and! or variability of absorption of bovine IgG.
This is the first demonstration of a foreign
pro-tein in human milk in concentrations comparable
with the concentrations found in infant formulas (Figure and Table 2). In the context of previous
studies,7’8 these findings raise the question of
whether bovine
IgG
might play a role in the etiology of infant colic. Results of some previous studies of breast-fed infants with colic and their mothers havebeen interpreted to mean that a cow’s milk protein
TABLE 2. Bovine IgG Content of Standard Cow’s Milk Infant Formula Preparations*
Product Type of Formula Bovine IgG, tg/mL
Enfamil (Mead Johnson and Ready-to-use 4.4, 4.6, 4.9, 6.4
Co, Evansville, IN) Concentrate Powder
0.9, 2.5 72, 110, 128
Similac (Ross Laboratories, Co- Ready-to-feed i.3, 2.6, 3.9, 4.5
lumbus, OH) Concentrate
Powder
0.8, 1.4
2.6, 3.i, 3.3, 5.2
SMA (iron fortified) (Wyeth Ready-to-feed 2.4, 3.5, 4.2 Laboratories, Philadelphia, Concentrate 0.6, 1.0
PA) Powder 1.5
* Each value represents a determination for one lot number of purchased formula. All lots
of the formulas available in the St Louis area were purchased and analyzed. Values are
given for concentrates and powders diluted according to manufacturers’ recommendations.
Iron-fortified and low-iron varieties of Enfamil and Similac were tested and had similar
bovine IgG levels. Bovine IgG was not detectable in any soy-based (Isomil and RCF, both
ARTICLES 443 (presumably absorbed by mothers from dietary
sources and transferred in breast milk to infants)
was implicated in the etiology of the infant colic.7’8 After ingestion ofwhey protein capsules by mothers of previously colicky infants, 9 of 10 breast-fed
infants demonstrated recurrences of colic in a
dou-ble-blind placebo-controlled study.8 However, the causative protein was not identified. The implica-tion that bovine 9-lactoglobulin might cause infant colic9 is difficult to reconcile with the following observations: (i) human milk contains nanogram
per milliliter concentrations of bovine
fi-lactoglobulin9’2; (2) cow’s milk formulas contain concentrations of 3-1actog1obulin in the milligram per milliliter range; and (3) the prevalence of infant colic is approximately 20% in both formula-fed and breast-fed infants.3’4 On the other hand, the hy-pothesis that bovine IgG may be an etiologic factor
in colic would be a tenable hypothesis consistent with previous and present observations.
We have found significantly higher
concentra-tions of bovine
IgG
in milk from mothers of colickyinfants compared with breast milk from mothers of noncolicky infants. This association supports, but does not prove, our hypothesis that bovine IgG may be one possible etiologic factor in colic. It should be noted that we are examining only one potential
factor, the bovine IgG concentration in human
milk. We are not testing other potentially impor-tant variables, eg, the infant’s ability to absorb (or to react to) bovine IgG, nor have we attempted yet
an interventional study. In considering the
poten-tial clinical significance of our testable hypothesis, one might explain why maternal avoidance of dairy products for i week results in improvement of colic in most breast-fed infants.7’8 The persistence of colic in some instances7’8’25 might have several pos-sible explanations: (i) dairy products were not strictly avoided25; (2) maternal levels of bovine IgG
were so high or half-life of bovine IgG was so long
that 2- to 7-day trials were sometimes insufficient; or (3) other etiologic factors may be involved. In considering treatment of colic in infants fed cow’s milk-based formula by switching to a casein hy-drolysate formula,2 the prolonged half-life of bovine
IgG might explain why short dietary trials may not give conclusive results.
ACKNOWLEDGMENTS
This study was supported by National Institutes of
Health grants P50 AI15322 and ROi A124005.
We thank Dr Kathleen Winters for enthusiastic help in obtaining breast milk samples and evaluation of in-fants in her practice. We are indebted to the St Louis Chapter of the La Leche League and to Dr Pat Wolff and
the physicians and assistants of the Health Key Medical
Group for assisting us in collecting milk samples. We are
grateful to Dr Charles Janeway (Yale University, New
Haven, CT) for advice in tolerizing rabbits during
im-munization and Dr Arthur Hirata (Abbott Labs, North
Chicago, IL) and Dr Renata Cathou (Technical
Evalua-tions, Lexington, MA) for advice on solid-phase RIA protocols. We acknowledge Michael A. Province
(Wash-ington University, Division ofBiostatistics) for statistical
analysis of the data and Carolyn Davinroy for secretarial assistance. We thank Dr John E. Butler (University of Iowa, Iowa City, IA) for helpful discussions and Drs
Harvey R. Colten and Charles W. Parker for reviewing
the manuscript.
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NEW
ELEMENT
DISCOVERED
The heaviest element known to science was recently discovered by physicians at Whatsamata U. The element, tentatively named Administratium, has no protons or electrons and thus has an atomic number of 0. However, it does have
i neutron, i25 assistant neutrons, 75 vice-neutrons and iii assistant vice-neutrons. This gives it an atomic mass number of 3i2. These 3i2 particles are held together in the nucleus by meson-like particles called memos. Since it has
no electrons, Administratium is inert. However, it can be detected chemically
as it impedes every reaction it comes in contact with.
According to the discoverers, a minute amount of Administratium caused one reaction to take 4 days to complete when it would normally take i second.
Administratium has a normal half-life of approximately 3 years, at which time it does not actively decay, but instead undergoes a reorganization in which assistant neutrons, vice-neutrons and assistant vice-neutrons exchange places. Some studies have shown that atomic mass number actually increases after reorganization.
Research at other laboratories indicates that Administratium occurs naturally
in the atmosphere. It tends to condense and concentrate at certain points such
as government agencies and universities, and can usually be found in the newest, best-appointed and best-maintained buildings.
Scientists point out that Administratium is known to be toxic at any level of
concentration, and can easily destroy any productive reaction where it is allowed
to accumulate. Attempts
are
being made to determine how Administratium can be controlled to prevent irreversible damage, but results to date are notprom-ising.
1991;87;439
Pediatrics
Patrick S. Clyne and Anthony Kulczycki, Jr
Human Breast Milk Contains Bovine lgG. Relationship to Infant Colic?
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1991;87;439
Pediatrics
Patrick S. Clyne and Anthony Kulczycki, Jr
Human Breast Milk Contains Bovine lgG. Relationship to Infant Colic?
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