Caffarelli et al.

Italian Journal of Pediatrics 2010, 36:5

http://www.iponline.net/content/36/1/5
!"#I"$ %pen &ccess
Cow's (il) protein aller*+ in children: a
practical *uide
Carlo Caffarelli
1,
, -rancesco .aldi
2
, .ar/ara .endandi
3
, 0ui*i Cal1one
2
, 3iris 3arani
5
,
Pa(ela Pas4uinelli
6
, on /ehalf of "$5P&5
&/stract
& oint stud+ *roup on cow's (il) aller*+ was con6ened /+ the "(ilia7!o(a*na $or)in* 5roup for Paediatric
&ller*+ and /+ the "(ilia7!o(a*na $or)in* 5roup for Paediatric 5astroenterolo*+ to focus /est practice for
dia*7nosis, (ana*e(ent and follow7up of cow's (il) aller*+ in children and to offer a co((on approach for
aller*olo7*ists, *astroenterolo*ists, *eneral paediatricians and pri(ar+ care ph+sicians.
8he report prepared /+ the stud+ *roup was discussed /+ (e(/ers of $or)in* 5roups who (et three ti(es in
Ital+. 8his *uide is the result of a consensus reached in the followin* areas. Cow's (il) aller*+ should /e
suspected in children who ha6e i((ediate s+(pto(s such as acute urticaria/an*ioede(a, whee1in*, rhinitis,
dr+ cou*h, 6o(itin*, lar+n*eal ede(a, acute asth(a with se6ere respirator+ distress, anaph+la9is. 0ate
reactions due to cow's (il) aller*+ are atopic der(atitis, chronic diarrhoea, /lood in the stools, iron deficienc+
anae(ia, *astroesopha*eal reflu9 disease, constipation, chronic 6o(itin*, colic, poor *rowth :food refusal;,
enterocolitis s+ndro(e, protein7los7in* enteropath+ with h+poal/u(ine(ia, eosinophilic
oesopha*o*astroenteropath+. &n o6er6iew of accepta/le (eans for dia*nosis is included. &ccordin* to
s+(pto(s and infant diet, three different al*orith(s for dia*nosis and follow7up ha6e /een su**ested.
Introduction
Cow's milk protein allergy (CMPA) affects from 2 to 6%
of children, with the highest prevalence dring the first
year of age !"#$ A%ot &'% of children have %een shown
to resolve CMPA within the first year of age, (')*'%
within their fifth year !2,+#$ ,he rate of parent)reported
CMPA is a%ot - times higher than the real one in chil)
dren !-#$ .o, many children are referred for sspected
CMPA %ased on parent perception, symptoms sch as
ctaneos erption, insomnia, persistent nasal o%strc)
tion, se%horreic dermatitis or positive reslts to
northodo/ investigations$ Moreover, parents often pt
their children on nnecessary diet withot an ade0ate
medical and dietary spervision$ ,hese inappropriate
dietary restrictions may provoke ntritional n%alances,
especially in the first year of age$ ,herefore, an accrate
diagnosis of CMPA is important in order to avoid not only
the risk of rickets, decreased %one minerali1ation !&#,
anaemia, poor growth and hypoal%minemia, %t
, Correspondence: carlo.caffarelli<unipr.it
1
=iparti(ento dell'"t> "6oluti6a, Clinica Pediatrica ?ni6ersit> di
Par(a, Par(a, Ital+
also that of immediate clinical reactions or severe chronic
gastroenteropathy leading to mala%sorption$
2ecently, three gidelines !6) (# reporting different
approaches to the infant with CMPA have %een p%lished$
3n view of these considerations, a stdy grop with
e/pert representatives of 4milia)2omagna 5orking 6rop
for Paediatric Allergy and of that for Paediatric
6astroenterology (456P6A), was constitted$ As
mmem%ers of the e/pert panel, the athors were assigned
to review practice with regard to diagnosis, management
and follow)p of CMPA for %oth comm)nity and hospital
paediatrician in order to share the same approach towards
the child$ ,he docment pre)pared %y the stdy grop was
%ased on e/isting recom)mendations, clinical e/perience
and evidence from the literatre$ ,he report was discssed
and received inpt %y the mem%ers (see participant list in
acknowledg)ments) of 456P6A which inclded
clinicians e/peri)enced in paediatric allergy, paediatric
gastroenterology and general paediatricians, in three
meetings held in 7ovem%er 2''(, 8e%rary 2''* and
March 2''* and a consenss was reached$ According to
the symptoms and
@ 2010 Caffarelli et alA licensee .io3ed Central 0td. 8his is an %pen &ccess article distri/uted under the ter(s
of the Creati6e Co((ons &ttri/ution 0icense :http://creati6eco((ons.or*/licenses//+/2.0;, which per(its
unrestricted use, distri/ution, and reproduction in an+ (ediu(, pro6ided the ori*inal wor) is properl+ cited.
Caffarelli et al. Italian Journal of Pediatrics 2010, 36:5 Pa*e 2 of B http://www.iponline.net/content/36/1/5
the type of infant diet, three different algorithms for
diagnosis and follow)p have %een sggested$ ,hese
approaches refer to the child in the first year of age$
2ecommendations for older children have %een %riefly
reported$
Cow's (il) protein aller*+: when should we
dou/tC
A positive atopic familiar history is common in children
with sspected CMPA !*#$ ,he diagnosis of CMPA is
%ased on a detailed history of symptoms (8ig$ "), skin
prick test and serm specific 3g4 to cow's milk protein,
elimination diet and oral food challenge$ Clinical mani)
festations de to CMPA !6) "-# can %e divided into 3g4)
mediated immediate clinical reactions (onset of the
symptoms within the +' mintes after the ingestion of
cow's milk) and non 3g4)mediated delayed reactions
(hors)days after food ingestion), most affecting the skin
and the gastrointestinal system$ 9owever, immediate and
delayed reactions can %e associated in atopic ec1ema and
in eosinophilic oesophageal gastroenteritis (8ig$ ")$
,he negative predictive vale of skin prick test:specific
3g4 for immediate reaction is e/cellent (;*&%) !"&#,
however a small nm%er of these patients can have clin)
ical reaction$ ,herefore, despite negative 3g4 tests if there
is a strong sspicion of CMPA, an oral food
challenge is necessary to confirm the a%sence of clinical
allergy$ <n the other hand, a%ot 6'% of children with
positive 3g4 tests have CMPA !"&,"6#$ Prick %y prick test
with cow's milk s%stittes may %e considered$
<ral food challenge, open or %lind, remains the Dgold
standardE to definitely ascertain children with food allergy
when the diagnosis is nclear !"=#$ <8C shold %e
performed nder medical spervision in a setting with
emergency facilities, especially in case of positive skin
prick test or serm specific 3g4 to cow's milk and in
infants at risk of an immediate reaction$
Cow's (il) su/stitutes
A%ot "'% of children with CMPA react to e/tensively
hydroly1ed formla (e98) !=#$ 3n comparison with e98,
soy formla (.8) provokes more fre0ently reactions in
children with CMPA aged less than 6 months !"(# %t not
in older children$ .8 mainly indces gastrointestinal
symptoms$
Amino acid formla (AA8) is non allergenic !"*#$ 3ts
se is limited %y the high cost and %ad taste$
2ice is allergenic and is often involved in the onset of
enterocolitis syndrome in Astralian infants !2'#$ Con)
trasting data have %een reported on the effect of protein
content on growth !2"#$ 3n 3talian children, rice formla
has %een shown to %e tolerated %y children with CMPA
!22#$ >arger long)term stdies are warranted to clarify
-i*ure 1 I((ediate and late onset reactions in children with cow's (il) protein aller*+.
Caffarelli et al. Italian Journal of Pediatrics 2010, 36:5 Pa*e 3 of B http://www.iponline.net/content/36/1/5
the se of rice formla in infants with CMPA$ 2ice for)
mla may %e a choice in selected cases taking into con)
sideration the taste and the cost$
9ome)made meals may %e a dietary option after -
months of age$
Mammalian milks are not ntritionally ade0ate$ 6oat's
milk commonly provokes clinical reactions in more than
*'% of children with CMPA !2+#, donkey's milk in a%ot
"&% !2-,2&# and has a high cost$
& child fed with cow's (il) for(ula with (ild7
(oderate s+(pto(s :-i*. 2;
3n infants with immediate symptoms (vomiting, acte
hives, angioedema, whee1ing, rhinitis, dry cogh) or late
symptoms (moderate:severe atopic dermatitis, diarrhoea,
%lood in the stools, iron deficiency anaemia, gastroeso)
phageal refl/ disease (6<2?), constipation) a CMPA
can %e sspected !6) (,"') "-#$ <ther cases are to %e
considered for patients nresponsive to treatment$ 3nfant
colic (more than + hors of crying a day, + days for more
than + weeks) is not nanimosly considered as a
conse0ence of CMPA$ ,he paediatrician has to consider
the opportnity of a cow's milk free diet in the most
tro%lesome cases !26,2=#$ Mild immediate
reactions may %e of difficlt interpretation %ecase they
can %e the reslt of cases different from CMPA$ 9ow)
ever, if these symptoms are strongly related to cow's milk
ingestion, we recommend to eliminate cow's milk and
follow the algorithm for severe reactions (8ig$ 2)$
2egarding delayed onset gastrointestinal symptoms,
other pathologies (i$e$ infections) shold %e e/clded
%efore investigating allergic sensiti1ation$
3n mild atopic dermatitis, investigations for CMPA are
not necessary in the a%sence of a clear relation %etween
cow's milk intake and onset of symptoms$
5hen a CMPA is sspected, infants shold go on a 2)-
week diet withot cow's milk protein$ 8or weeks shold
%e considered for chronic gastrointestinal symp)toms$
3nfants shold %e fed with e98 or .8 in children aged
more than 6 months and withot gastrointestinal
symptoms$
3f the symptoms improve on a restrict diet, an <8C to
cow's milk is necessary to definitely ascertain the diag)
nosis$ 3f the oral food challenge is positive, the child mst
follow the elimination diet and can %e re)chal)lenged after
6 months (a shorter period for 6<2?) and in any case,
after *)"2 months of age$ 3f the oral food challenge is
negative, a free)diet can %e followed$
Children less than 1 year fed with regular cows milk formula with suspected mild-moderate CMPA
Immediate reactions with unclear history*: Late reactions
Test: Vomiting Atopic dermatitis (moderate/severe)*
SPT, Acute orticaria, angioedema Diarrhoea, stool blood, iron defciency anaemia,
specifc IgE Wheezing, rhinitis, dry cough GORD, constipation (with exclusion of other causes)
*If history is clear, exclusion diet is requested, Infantile colic
challenge is not necessary (see severe *mild atopic dermatitis: no restrict diet is requested if
symptoms) there is negative history of reactions to cows milk.
Elimination diet for 2-4 week (4 weeks for gastrointestinal symptoms):
Extensively hydrolyzed formula
Soy formula if >6 months of age (without gastrointestinal symptoms)
Test:
SPT, specifc
IgE, stool
eosinophils or
stool blood
Positive IgE
test with
history of
strongly
related
clinical
reaction
Yes Improves ? No
Oral food challenge (consider to perform Positive Negative IgE test
challenge test in a clinical setting in case IgE test Atopic dermatitis
of positive specifc IgE and/or SPT)
Positive
Avoid cows milk for at least 6 months
and until 9-12 months of age (assess a
shorter period in GORD).
Amino acid
Negative formula
Not
better
Regular cows Oral food challenge Regular
milk should be considered if it cows milk
formula is successful formula
-i*ure 2 &l*orith( for children F 1 +ear fed with cow's (il) for(ula and (ild7(oderate s+(pto(s.
Caffarelli et al. Italian Journal of Pediatrics 2010, 36:5 Pa*e 2 of B http://www.iponline.net/content/36/1/5
5hen there is strong sspicion of 3g4)mediated reac)tions, in
infants who do not respond to a diet with e98 or .8 an attempt
may %e made with a "-)days diet with AA8$
Cow's milk s%stittes are sed in children aged less
than "2 months$ 3n older children with CMPA, e98 or
AA8 are not sally necessary %ecase an ade0ate diet is
easily accessi%le$
& child fed with cow's (il) for(ula with se6ere
s+(pto(s :-i*. 3;
3mmediate severe symptoms are considered laryngeal
edema, acte asthma with severe respiratory difficlty,
anaphyla/is$ ,he following are delayed onset severe
symptoms@ chronic diarrhoea or chronic vomiting with
poor growth, intestinal %leeding with iron deficiency
anaemia, protein losing enteropathy with hypoal%mine)
mia, eosinophilic gastroenteropathy confirmed %y %iopsy
!=,(,"') "-#$
3f any of these immediate symptoms are o%served as a
conse0ence of sspected CMPA, infants shold follow a
cow's milk free diet$ As s%stittes, .8 (if older than 6
months of age) or e98 or AA8 can %e sed$ e98 and .8
shold %e started nder medical spervision %ecase
of possi%le clinical reactions$ 3f an AA8 is adopted, it may
%e administered for 2 weeks and then the infant may %e
switched to .8 or e98$
3n children with late severe gastrointestinal symptoms
with poor growth, anaemia or hypoal%minemia or eosi)
nophilic oesophagogastroenteropathy, it is recom)mended
to start an elimination diet with AA8 and then switched
with e98$ ,he effect of the diet shold check ot within
"' days for enterocolitis syndrome, ")+ weeks for
enteropathy and 6 weeks for eosinophilic
oesophagogastroenteropathy$
3n children with anaphyla/is and concordant positive
3g4 tests or severe gastrointestinal reactions, oral food
challenge is not necessary for diagnosis$ ,he oral food
challenge for tolerance ac0isition shold %e performed
not %efore 6)"2 months after the last reaction$ Children
have to eliminate cow's milk ntil "2 months of age, %t
in those with enterocolitis syndrome ntil 2)+ years of age
!2(#$
Children with any severe symptoms shold %e referred
to a speciali1ed centre$
e98 or AA8 is sed in children aged less than "2
months and in older children with severe gastrointestinal
-i*ure 3 &l*orith( for children F1 +ear fed with cow's (il) for(ula and se6ere s+(pto(s. In child less than1 +ear of a*e, infant
for(ula is not co(pulsor+.
Caffarelli et al. Italian Journal of Pediatrics 2010, 36:5 Pa*e 5 of B http://www.iponline.net/content/36/1/5
symptoms$ 3n children ; "2 months with anaphyla/is,
cow' s milk s%stittes are not always ntritionally
re0ired$
& /reast7fed infant with a suspected C3P& :-i*. 2;
3n e/clsively %reast)fed infants, sspected symptoms to
the cow's milk proteins are almost always non 3g4)
mediated as atopic dermatitis, vomiting, diarrhoea, %lood
in the stools, 6<2?, colic !2*#$
A maternal diet withot cow's milk is not recom)
mended for mild symptoms$
,here is no evidence that a maternal diet withot egg
and cow's milk in infants with %loody stools (proctocoli)
tis) is of vale !+',+"#$
3n infants with moderate)severe symptoms, cow's milk
protein, eggs and other foods shold %e eliminated %y the
mother's diet only if history sggests an ne0ivocal
reaction$ Moreover, the infant shold %e referred to a
speciali1ed centre$ ,he maternal elimination diet has to %e
followed for - weeks$ 3f there is no improvement the diet
shold %e stopped$ 3f symptoms improved, it's
recommended that the mother ingested large amonts of
cow's milk for one week$ 3f symptoms occrred, the
mother will contine the diet with spplemental intake of
calcim$ ,he infant can %e weaned as recommended for
healthy children, %t cow's milk shold %e avoided ntil
*)"2 months of age and for at least 6 months from the
%eginning of the diet$ 3f the volme of %reast milk is
insfficient, e98 or .8 formla (if ; 6 months) shold %e
administered$
3f after the reintrodction of cow's milk in mother's diet
symptoms do not occr, the e/clded foods can %e
introdced one %y one in the diet$
Conclusions
,he diagnosis of CMPA is %ased on oral food challenge
that follows a 2)- week elimination diet$
A diagnostic oral food challenge is nnecessary in
immediate reactions or late gastrointestinal reactions with
anaemia, poor growth or hypoal%minemia if the
casative role of cow's milk is clear$ Children can %e
challenged after 6)"2 months from the reaction and
Breast-fed infants with suspected reactions to cows milk: atopic dermatitis,
vomiting, diarrhoea, stool blood, GORD, poor growth, infantile colic.
Clinicalevaluation, family history
Mild symptoms Moderate-severe smptoms
SPT/specifc IgE,
No Maternal diet without
stool
eosinophils or stool
diet cows milk for 2-4 weeks.
blood.
Improves ?
No Yes
Free Give cows
maternal milk to the
diet mother for 1
week.
Symptoms ?
No
When it is necessary, breastfeeding should Yes
be supplemented with extensively
Exclusion Free
hydrolyzed formula or soy formula (if > 6
diet maternal
months).
diet
Food challenge test after 6-12 months of
avoidance.
-i*ure 2 &l*orith( for /reast7fed infants with suspected non7I*" (ediated reactions to cow's (il) protein.
Caffarelli et al. Italian Journal of Pediatrics 2010,
36:5 http://www.iponline.net/content/36/1/5
not %efore "2)2- months of age according to the
symptoms$
?iets mst %e ntritionally %alanced$ 3n children with
CMPA, a spplementation with calcim mst %e
evalated$
?iet is not re0ested in children with mild atopic der)
matitis and negative history for cow's milk reactions$
.8 shold not %e sed in infants A 6 months of age with
allergic symptoms and in those with late gastroin)testinal
symptoms$
Children with gastrointestinal reactions and anaemia,
poor growth or hypoal%minemia shold %e given AA8
and then switched to e98$
e98 or AA8 is sed in children aged less than "2
months and in older children with severe gastrointest)inal
symptoms$ 3n children ; "2 months with anaphy)la/is,
cow's milk s%stittes are not always ntritionally
re0ired$
0ist of a//re6iations
CMPA@ cow's milk protein allergyB 456PA6@ 4milia)
2omagna 5orking 6rop for Paediatric Allergy and of
that for Paediatric 6astroenterologyB e98@ e/tensively
hydroly1ed formlaB .8@ soyB AA8@ amino acid formlaB
6<2?@ gastroesophageal refl/ disease$
&c)nowled*e(ents
Ph+sicians and specialists of "(ilia7!o(a*na "(ilia7!o(a*na
$or)in* 5roup for Paediatric &ller*+ and for Paediatric
5astroenterolo*+ :"$5P5&; who contri/uted to this *uide.
Paediatric *astroenterolo*+: Patri1ia &l6isi :?.%. di Pediatria %spedale
3a**iore, .olo*na, Ital+;, Ger*io &(arri :?.%. di Pediatria, !e**io "(ilia, Ital+;,
Paolo .aldassarri :?.%. di Pediatria, -orlH,;, Gandra .rusa :?.%. di Pediatria,
I(ola, Ital+;, 3arisa Calacoci :Pediatra 0i/ero Professionista, -errara, Ital+;,
Iliana Cecchini :?.%. di Pediatria, Cesena, Ital+;, Gara =enti :?.%. di Pediatria,
Carpi, Ital+;, &nnarita =i .iase :?.%. di Pediatria, 3odena, Ital+;, Cristina Iost
:?.%. di Pediatria, -errara, Ital+;, &ndrea 0a(/ertini :?.%. di Pediatria %spedale
3a**iore, .olo*na, Ital+;, &n*elo 3iano :Pediatra 0i/ero Professionista,
Cesena, Ital+;, &nna(aria 3etri :?.%. di Pediatria, -aen1a, Ital+;, 3arco %ccari
:?.%. di Pediatria, 3anto6a, Ital+;, !en1o Pini :?.%. di Pediatria, !i(ini, Ital+;,
3arina !ossidoria :Pediatra 0i/ero Professionista, .olo*na, Ital+;. Paediatric
aller*+: &ndrea #alenti :?.%. di Pediatria, 0u*o, Ital+;, 3onica #allini :Pediatra
0i/era scelta, .olo*na, Ital+, Ital+;, Iole #enturi :?.%. di Pediatria, !a6enna,
Ital+;, 0aura #iola :?.%. di Pediatria, !i(ini, Ital+;. "r(anno .aldo :?. %.di
Pediatria, !o6ereto, Ital+;, 3auro .andini :?.%. di Pediatria, !a6enna, Ital+;,
-ilippo .ernardi :Clinica Pediatrica %spedale G. %rsola, .olo*na, Ital+;, &driana
.or*hi :?.%. Pediatria, Carpi, Ital+;, Paolo .ottau :?.%. di Pediatria, I(ola, Ital+;,
0ucetta Capra :?.%. di Pediatria &1ienda %spedaliera7?ni6ersitaria G. &nna,
-errara, Ital+;, 5io6anni Ca6a*ni :%spedale Pediatrico .a(/in 5esJ, !o(a,
Ital+;, 3atteo Corchia :Clinica Pediatrica, Par(a, Ital+;, =anilo =alpo11o :?.%.di
Pediatria, I(ola, Ital+;, 0eonardo 0oroni :?.%. di Pediatria, !a6enna, Ital+;,
0aura 5io6annini :Pediatra 0i/ero Professionista, 0u*o, Ital+;, 3assi(o 3asi
:=iparti(ento KGalute della donna, del /a(/ino e dell'adolescente, Policlinico G.
%rsola73alpi*hi, .olo*na, Ital+;, 5iuseppe 3enna :IGG Istituto Gicure11a
Gociale, ?.%.C.Pediatria7%spedale della !epu//lica di Gan 3arino, Ital+;,
Patri1ia Preti :?.%. di Pediatria %spedale 3a**iore, .olo*na, Ital+;, 5ia(paolo
!icci :=iparti(ento KGalute della donna, del /a(/ino e dell'adolescente,
Policlinico G. %rsola73alpi*hi, .olo*na, Ital+;, 5iuseppe 8i(oncini :?.%. di
Pediatria, -orlH, Ital+;, 0oretta .iserna :?.%. di Pediatria, !a6enna, Ital+;, "lena
La(uner :?.%. di Pediatria, !a6enna, Ital+;.
Pa*e 6 of B
&uthor details
1
=iparti(ento dell'"t> "6oluti6a, Clinica Pediatrica ?ni6ersit> di Par(a,
Par(a, Ital+.
2
?% di Pediatria, &?G0 I(ola, I(ola, Ital+.
3
=iparti(ento
KGalute della donna, del /a(/ino e dell'adolescenteE Policlinico G %rsola7
3alpi*hi, Clinica Pediatrica, .olo*na, Ital+.
2
=iparti(ento "(er*en1a ed
&ccetta1ione dia*nostica, ?% di Pediatria, -iden1a, Ital+.
5
Pediatria, &?G0
di !a6enna, Ital+.
6
?% Pediatria, &?G0 di Cesena, Ital+.
&uthors' contri/utions
CC, -., .., 0C, 33, PP concei6ed the desi*n of the stud+ and
participated in its coordination. 8he+ prepared the draft of the (anuscript
and re6ised it. &ll authors read and appro6ed the final (anuscript.
Co(petin* interests
8he authors declare that the+ ha6e no co(petin* interests.
!ecei6ed: 11 =ece(/er 200M
&ccepted: 15 Januar+ 2010 Pu/lished: 15 Januar+ 2010
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Cite this article as: Caffarelli et al.: Cow's (il) protein aller*+ in
children: a practical *uide. Italian Journal of Pediatrics 2010 36:5.
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