Allergy to cow's milk is the most common food allergy in childhood and is experienced, albeit less frequently, in adults. There is an extensive literature on cow's milk allergy and only a summary is listed below.
Cow's milk allergy differs from, for example, allergy to nuts or crustacea, in that allergy generally develops before age 3 and that fortunately most sufferers become tolerant to milk within a few years. Thus it is not surprising that the distribution of symptoms may be different with, for example, more cases of atopic dermatitis associated with milk allergy.
Besler et al. (2002) [1499] in a review of more than 20 articles lists symptoms to cow's milk as follows:
Several additional symptoms such as failure to thrive are also associated with allergy to milk, reflecting the age of onset.
Skin Prick Test
Number of Studies:
>20
Food/Type of allergen:
Plaza Martin et al (2001) [1198] used alpha-lactalbumin or beta-lactoglobulin (5 mg/ml) and casein (10 mg/ml) (all from CBF Leti, Barcelona, Spain). A result was considered positive when the test produced a skin weal of 3 mm or more in diameter.
Sporik et al. (2000) [1322] and Hill et al. (2001) [662] used a commercial milk extract.
Protocol:
(controls, definition of positive etc)
Plaza Martin et al (2001) [1198] considered the test positive when a skin weal was 3 mm or more in diameter.
Sporik et al. (2000) [1322] and Hill et al. (2001) [662] used a positive, histamine, 1 mg/ml, and a negative control solution. Tests were performed on the patients' backs. The skin weal diameter was measured after 10-15 min for histamine and after 15-20 min for test materials. The results with different diameters were discussed.
Number of Patients:
Plaza Martin et al (2001) [1198] tested 49 infants aged less than 6 months and retested them at age 1 year.
Hill et al. (2001) [662] tested 640 patients with milk extract. The patients were aged below 2 years.
Sporik et al. (2000) [1322] reported the SPT wheal diameters for 339 patients with milk (from 467 children with suspected food allergies with median age 3.0 years).
Summary of Results:
Vanto et al. (2004) [1508] found that the size of the SPT wheal was predictive of the development of tolerance. A wheal size of <5 mm in SPT correctly identified 83% of 124 infants who developed tolerance by aged 4 years, and a wheal size of >5 mm in SPT correctly identified 71% of 39 infants with persistent allergy.
Hill et al. (2001) [662] found that 125/640 patients gave positive SPT defined as 6 mm diameters. Comparison with IgE tests on sera for SPT positive patients showed that 20, 14, 29, 61 and 1 had 0 - 0.34, 0.35 - 0.69, 0.7 - 3.49, 3.5 - 17.5 and >17.5 kU/l respectively (or AEU/ml for pre-1999 tests).
Plaza Martin et al (2001) [1198] found that positive SPT predicted all positive oral challenges with immediate reactions. Positive challenges following negative SPTs were associated with delayed reactions.
Sporik et al. (2000) [1322] found that all patients with SPT wheal diameters >8 mm were allergic. At 3 mm, approximately equal numbers were challenge positive and negative. They recommend 6 mm as confirming allergy, so that challenge is unnecessary.
IgE assay (by RAST, CAP etc)
Number of Studies:
>20
Food/Type of allergen:
Commercial extracts.
IgE protocol:
Celik-Bilgili et al. (2005) [1309], Perry et al. (2004) [1218], Shek et al. (2004) [1214], Szabo & Eigenmann (2000) [1068] and Sicherer & Sampson (1999) [1208] used the Pharmacia CAP System FEIA.
Szabo & Eigenmann (2000) [1068] used ELISA for IgG determination.
Number of Patients:
Perry et al. (2004) [1218] measured IgE levels to milk in 159 children who were subjected to oral challenge with milk.
Shek et al. (2004) [1214] repeatedly measured IgE levels in 49 children who were also subjected to oral challenge with milk.
Sicherer & Sampson (1999) [1208] measured IgE levels to milk in sera from 64 children. These were divided into 4 groups: 30 under age 3 at time of positive oral challenge or anaphylactic reaction; 20 over age 9 at the time of positive oral challenge or anaphylactic reaction; 11 with samples from before tolerance was achieved; 16 samples from patients after they lost sensitivity with 9 paired samples between groups 3 and 4.
Summary of Results:
Sicherer & Sampson (1999) [1208] reported that no single allergen dominanted IgE binding patterns. However, those with persistent allergy over age 9 years had significantly elevated levels of milk and casein-specific IgE compared with younger children. These results were consistent with the results of previous studies. In detail, all allergic children had detectable casein and whey-specific IgE. Beta-lactoglobulin-specific IgE was undetectable in 7/30 (23%) in Group I, 7/20 (35%) in Group II and in 5/11 (45%) of the children in Group III. Alpha-lactalbumin-specific IgE was undetectable in 5/30 (17%) in Group I, 6/20 (30%) in Group II, and in 5/11 (45%) of Group III. Bovine serum albumin-specific IgE was undetectable in approximately 50% of each group.
Szabo & Eigenmann (2000) [1068] report that sera from the cow's milk-allergic patients contained specific IgE concentrations to milk ranging from 8.2 to 4225 IU/ml, with a median of 39.8 IU/ml. Both allergic patients and controls had similar IgG levels to milk.
Perry et al. (2004) [1218] report that 11/34 patients with a history suggestive of allergy with specific IgE <0.35 KU/l were positive on challenge, 31/56 with 0.35 - 2 KU/l were positive, 20/32 with 2 - 3 KU/l were positive and 26/31 with >3 KU/l. Of 6 patients with an unclear history, 1/2 with <0.35 KU/l and 1/2 with 0.35 - 2 KU/l were positive on challenge but 2 with >3 KU/l did not react.
Shek et al. (2004) [1214] determined the probability of developing tolerance to milk based on the % decrease in specific IgE over 12 months as 0.31 (50% reduction), 0.45 (75% reduction), 0.66 (90% reduction) and 0.94 (99% reduction) for children diagnosed before age 4. In total 16 children became tolerant and 33 remained allergic. No clear relationships predicting tolerance were seen in children first diagnosed with food allergy when older than 4 years although only 6 fell into this category.
Celik-Bilgili et al. (2005) [1309] found a correlation between the measured IgE levels to milk and the probability of a positive challenge. However, only the 21 patients with >50 kU/l were all challenge positive. Most patients had lower levels of specific IgE: 141 with <0.35 kU/l, 46 with 0.35-0.7 kU/l, 87 with 0.7-3.5 kU/l, 61 with 3.5-17.5 kU/l and 41 with 17.5-50 kU/l and approximate probabilities of 0.23, 0.43, 0.5, 0.7 and 0.75 respectively.
Sampson (2001) [651] described a decision point with a 95% predicted probability of a positive DBPCFC of 15 kU/l specific IgE to cow's milk in the US population whilst Garcia-Ara et al. (2001) [1328] reported 5 kU/l specific IgE to cow's milk as a 95% positive predicted value in Spanish infants. In contrast to these studies, no useful predictive decision points could be obtained for German children by Celik-Bilgili et al. (2005) [1309]. Lin et al. (1998) [1412] also reported >0.7 ku/l levels of IgE specific to proteins of cow's milk in sera from atopic children without clinical allergy to milk.
Immunoblotting
Immunoblotting separation:
Docena et al. (1996) [1408] separated proteins in 1D 14% polyacrylamide gels (Laemmli, 1970 [948]) with 35 µg per lane. 2-mercaptoethanol was used in some separations.
Szabo & Eigenmann (2000) [1068] used SDS PAGE with a Bio-Rad Mini Protean II (Bio-Rad, Richmond, CA, USA) at 80 V through the stacking gel, and at 160 V through the running gel. Cow's milk was run reduced by 2% beta-mercaptoethanol but unboiled.
Natale et al. (2004) [1409] used 1D electrophoresis using 12% NuPage ZOOM gels (Invitrogen) and 2D electrophoresis with IEF in 7M urea, 2M thiourea, 4% CHAPS, 0.2% BioLyte (Bio-Rad) either 3-6 or 3-10 NL, 65 mM DTT and traces of Bromo Phenol Blue, followed by treatment with 50 mM DTT, then 65 mM iodoacetamide and SDS PAGE in a 12% acrylamide gel.
Immunoblotting detection method:
Docena et al. (1996) [1408] electrotransferred proteins to 0.45 µm nitrocellulose membranes for 1 hour at 270 mA. The membranes were blocked with PBS containing 5% (v/v) horse serum and cut into strips. Strips were incubated with sera diluted 1/5 (v/v) in PBS for 12 hours at room temperature. After washing, the strips were incubated with anti-IgE (or anti-IgG) antibodies conjugated to alkaline phosphatase for 12 hours at room temperature. Binding was revealed with 5-BCIP/NBT substrate (Sigma).
Szabo & Eigenmann (2000) [1068] electrotransferred proteins to nitrocellulose (ProtranTM 0.2 µm). Blots were blocked for 1 h in phosphate buffered saline plus 0.05% (v/v) Tween (PBS-T) with 0.5% (w/v) gelatin and then incubated with serum and PBS-T (1:10 v/v dilution for IgE, 1:200 (v/v) for IgG, and 1:20 (v/v) for IgG4) for 2 h at room temperature on a rocking platform. Antibodies were bound by a goat anti-human IgE at 0.5 µg/ml (Kirkegaard and Perry, Gaitersburg, USA), or a sheep antihuman IgG (0.5 µg/ml) or a mouse antihuman IgG4 (1:1000 v/v) (Serotec Ltd, Oxford, UK). Five washes (for 5 min) with PBS-T were done between each step. The blots were developed with DABTM(Sigma).
Natale et al. (2004) [1409] electroblotted proteins onto 0.2 µm nitrocellulose (Sigma) in a semi wet module (Invitrogen). Membranes were blocked with tris buffered saline, pH 7.4, with 0.3% v/v Tween and incubated overnight with sera diluted 1:5 by the same buffer with 0.05% (v/v) Tween and 0.05% (w/v) gelatin (Bio-Rad). The membranes were rinsed with tris buffered saline with 0.03% (v/v) Tween and incubated with alkaline phosphatase-conjugated goat anti-human-IgE diluted 1:1000 (v/v) in the tris/Tween/gelatin buffer. Binding was revealed with BCIP/NBT (Bio-Rad).
Immunoblotting results:
Docena et al. (1996) [1408] report that serum IgE from 80/80 individuals bound to casein aggregates. 10/80 sera contained IgE against beta-lactoglobin and 5/80 against alpha-lactalbumin. Both IgE and IgG bound to masses >150 kDa and 60-70 kDa, which disappear on reduction, with IgE also reacting to alpha- or beta-caseins. If the high mass aggregates are reducted and treated with urea, some binding to aggregates and also to caseins remains. No IgE binding to bovine serum albumin was observed. In addition, inhibition experiments were used to rule out bovine serum albumin as the 60-70 kDa band and confirming IgE binding to caseins and beta-lactoglobin.
Szabo & Eigenmann (2000) [1068] reported serum IgE binding to the casein fractions in 9/10 cow's milk allergic individuals, to beta-lactoglobulin in 5/10 and to alpha-lactabumin in 2/10. IgG and IgG4 bound to the fractions in a very similar way to IgE, suggesting that allergy results from a failure of class switching.
Natale et al. (2004) [1409] used 20 sera from patients from 4 months to 14 months. They found that 55% of the individuals had serum IgE against alpha S1-casein, 90% against alpha S2-casein, 15% against beta-casein, 50% against kappa-casein, 45% against beta-lactoglobulin, 45% against bovine serum albumin, 95% against IgG heavy chain and 50% against lactoferrin, with none binding alpha-lactalbumin.
Oral provocation
Number of Studies:
>20
Food used and oral provocation
vehicle
Celik-Bilgili et al. (2005) [1309] gave doses of 0.1, 0.3, 1.0, 3.0, 10.0, 30.0, 100.0 mls of fresh pasteurized cow's milk (total 144.4 mls) or placebo (Neocate®, SHS, Liverpool, UK) at 20 min. intervals. The children were observed for 48 h after each challenge on an in-patient basis in order to detect late clinical reactions.
Perry et al. (2004) [1217] gave the food in escalating doses every 15 min. until 4 g (<5 years old) or 8 g (>5 years old) of milk protein had been ingested. The challenge was terminated on objective symptoms or when subjective symptoms such as abdominal pain worsened. Patients were observed in the clinic for a minimum of 4 hours or until signs of clinical reactivity subsided for those patients who failed the challenge and were instructed before discharge to contact a physician on possible late-phase reactions.
Plaza Martin et al (2001) [1198] gave up to 20 ml of adapted cow's milk protein formula (Nidina 1 ®, Nestle, Spain). Vital signs were monitored every 30 minutes during the first hour after formula intake and again every hour for 3 hours after the last dose administered in the challenge test. The infants were monitored for 24 hours after the challenge test.
Sporik et al. (2000) [1322] gave 1 drop of milk inside lip, 0.5, 2.5, 5, 10, 20, and 30 mLs at 30 minute intervals. On day 2: 30, 60 and 120 mLs at 30 minute intervals and on day 3: normal volumes of milk, i.e. > 450 mLs per day.
Blind?
Plaza Martin et al (2001) [1198], Perry et al. (2004) [1217] used open challenge.
Celik-Bilgili et al. (2005) [1309] used DBPCFC in general but open challenges for babies below 1 year in age.
Number of Patients?
Celik-Bilgili et al. (2005) [1309] challenged 398 children with cow's milk. Most showed symptoms of atopic dermatitis.
Plaza Martin et al (2001) [1198] challenged 49 infants aged less than 6 months and rechallenged those with negative SPT and negative tests for sera IgE after an exclusion diet at age 1 year.
Sporik et al. (2000) [1322] challenged 339 patients with cow's milk with a median age of 31 months. 120 were less than 2 years old.
Dose response
Taylor et al. (2002) [639] have collected data from several studies with the aim of defining thresholds for reaction to milk (299 patients in total). Studies have used liquid cow's milk, nonfat dry milk, or infant formula (Taylor et al, 2004) [1505]. The lowest provoking dose was 0.02 mL of milk, which was seen in 21 patients by open challenge.
Morrisset et al. (2003) [613] considering objective reactions apart from abdominal pain in children, found that 5% reacted to 0.8 mL of milk and 1.7% (2/59) reacted to the lowest reactive dose of 0.1 mL of milk.
Symptoms
Celik-Bilgili et al. (2005) [1309] reported that 49% of the milk challenges were positive. Symptoms for early reactions to milk, egg, wheat and soy were listed as urticaria (55%), gastrointestinal (14%), urticaria and gastrointestinal (22%), respiratory and gastrointestinal (1%), respiratory and urticaria (7%), and analphylaxis (1%). Few reactions to egg or milk were delayed reactions (mostly atopic dermatitis).
Perry et al. (2004) [1217] reported 90 out of 161 patients (56%) reacted to a challenge with milk. The median food-specific IgE for patients reacting was 2.0 kUA/L and the median percent of challenge food ingested was 25%. The symptoms in the clinical history of the 90 patients included eczema (60%), asthma (57%) and allergic rhinitis (47%). 89% suffered from another food allergy. Symptoms on challenge were cutaneous (68, 75%), oral (23, 26%), upper respiratory (16, 18%), lower respiratory (24, 27%) and gastrointestinal (37, 41%) with no cardiovascular symptoms reported. Reactions were classified as mild (33,37%), moderate (33, 37%) and severe (24, 27%). IgE levels to milk did not predict severity.
Plaza Martin et al (2001) [1198] reported immediate reactions in 92 % of the children at the time of diagnosis. Symptoms were rash in 63 %, vomiting in 43 %, anaphylaxis in 10 % and respiratory symptoms in 12 % (respiratory symtoms always occurred with other symptoms). 8% of the clinical reactions were late and all manifested as dyspepsia. On retesting at age 1 year, only 5 children (21%) presented a positive reaction which did not occur in the first 24 hours after the reintroduction of cow's milk protein to the diet.
Sporik et al. (2000) [1322] report 143 positive challenges to milk with urticaria (73%), eczema flare (7%), vomiting (14%), diarrhoea, colic or abdominal pain (21%), respiratory (14%) and rhinitis (15%).
IgE cross-reactivity and Polysensitisation
Bernard (1999) [1494] showed that in general the IgE of cow's milk allergic patients binds homologous proteins from milks from other species (e.g. cow, sheep, goat, rabbit and rat). Similarly, Restani et al. (1999) [1624] and Restani et al. (2002) [1480] reported that caseins, beta-lactoglobulin and serum albumins from buffalo, sheep and goat bind IgE from cow's milk allergic patients. Bellioni-Businco et al (1999) [1627] reported that 24/26 cow's milk allergic patients reacted to goat's milk on oral challenge. However, Businco et al (2000) [1628] report that most cow's milk allergic patients can tolerate mare's milk and Restani et al. (1999) [1624] suggest that camel's milk might be tolerated.
Other Clinical information
General surveys of methods used for oral challenges in hospitals have been published such as Martelli et al. (2005) [1504].
Karlsson et al. (2004) [1431] report that the induction of tolerance to cow's milk is associated with higher levels of circulating CD4(+)CD25(+) T cells.
Diagnosis of milk allergy by the atopy patch test (APT) has led to apparently conflicting results. Osterballe et al. (2004) [1340] conclude that the APT cannot be recommended in daily practice for the diagnosis of hypersensitivity to cow's milk and hen's egg in children 3 years of age. By contrast, Roehr et al. (2001) [1325] suggest that the combination of positive APT results and measurement of levels of specific IgE makes double-blind, placebo-controlled, food challenges superfluous for suspected cow's milk and hen's egg allergy.
Saarinen et al (2002) [1514] showed that infants with gasterointestinal symptoms on challenge with cow's milk, both those showing immediate and those with delayed symptoms, showed increased levels of fecal eosinophil cationic protein compared to those showing other symptoms. There was some overlap in concentrations of the mediators of inflamation between the allergic and tolerant infants, possibly because all were suspected of having reacted to milk.
Järvinen et al. (2002) [1192] found that patients with transient allergy showed only weak binding to alpha S2-casein peptides. By contrast, the binding of beta-lactoglobin peptides was stronger in the transiently allergics.
Martelli et al. (2002) [1479] reviews the link between cow's milk allergy and allergy to beef and other meats. Werfel et al. (1997) [1626] suggest that allergy to beef is rare because the allergenicity of bovine serum albumin and immunoglobulin gamma is generally destroyed if beef is well cooked.
The importance of milk in infant nutrition implies that exclusion diets generally require supplements to avoid deficiencies of calcium or vitamins (Jensen et al. 2004 [1633]; Fox et al. 2004 [1632]; Carvalho et al. 2001 [1631]; Davidovits et al. 1993 [1629]; Castile et al. 1975 [1630]).
Reviews (6)
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Bernhisel-Broadbent J, Yolken RH, Sampson HA.
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12373003
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12002741
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9276457
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11335767
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Chatchatee P, Jarvinen KM, Bardina L, Vila L, Beyer K, Sampson HA.
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11529896
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Docena GH, Fernandez R, Chirdo FG, Fossati CA.
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Garcia-Ara C, Boyano-Martinez T, Diaz-Pena JM, Martin-Munoz F, Reche-Frutos M, Martin-Esteban M.
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11150010
Hidvegi E, Cserhati E, Kereki E, Savilahti E, Arato A.
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Hill DJ, Heine RG, Hosking CS.
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Järvinen KM, Beyer K, Vila L, Chatchatee P, Busse PJ, Sampson HA.
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Järvinen KM, Chatchatee P, Bardina L, Beyer K, Sampson HA.
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Roehr CC, Reibel S, Ziegert M, Sommerfeld C, Wahn U, Niggemann B.
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