Clinical and Laboratory Studies

Dermatology 2009;218:119125 DOI: 10.1159/000165629

Received: March 10, 2008 Accepted: June 10, 2008 Published online: October 22, 2008

Patch Tests in Children with Suspected Allergic Contact Dermatitis: A Prospective Study and Review of the Literature
Flora B. de Waard-van der Spek Arnold P. Oranje
Paediatric Dermatology Unit, Department of Dermatology, Erasmus MC-Sophia Childrens Hospital, Rotterdam, The Netherlands

Key Words Allergic contact dermatitis Patch test, children, infants Sensitization Delayed-type allergy

Introduction

Abstract Aims: The results of patch testing in children visiting our outpatient clinic with suspected allergic contact dermatitis (ACD) were prospectively investigated and compared with those reported in the literature. A review of the literature on patch testing and ACD in children is provided. Methods: Children were patch tested using the TRUE test, supplemented with tixocortol-17-pivalate, budesonide and 3 commonly used emollients. Supplementary patch tests were undertaken on indication. Results: Seventy-nine children (31 boys and 48 girls) were patch tested. Of the patients tested, 40 (51%) had 1 or more positive allergic patch test reactions. Twenty-two (55%) of these 40 children suffered from atopic dermatitis, 9 (23%) from hand or foot dermatitis, and 9 (23%) from other skin ailments. Nickel was the most common contact allergen, but many other common and less common allergens were noted to give positive patch tests in patients. Conclusion: Sensitization to contact allergens may begin in infancy and continue to be more common in toddlers and young children. In recalcitrant atopic dermatitis, especially at the age of 5 years and over, patch tests are indicated. Good information on preventing the development of ACD in children is useful for caregivers. Copyright 2008 S. Karger AG, Basel

Allergic contact dermatitis (ACD) in children is not uncommon. The documented rates of ACD in children are on the increase. Sensitization to contact allergens begins in infancy and continues to be more common in toddlers and young children. Infants, even neonates, may be sensitized. The rate of positive results may vary with referral patterns, selection criteria for patch testing, regional and social variations in allergen exposure and the allergens tested. Reported rates of positive patch tests in series of children with suspected ACD have risen to 67% [1]. In this study we investigated prospectively the results of patch testing in children with suspected ACD visiting our out-patient clinic. Our results were compared with those reported in the literature, and a review of the literature on patch testing and ACD in children is provided.

Methods
Patients Seventy-nine children (31 boys and 48 girls aged 118 years, mean age 10 years) were patch tested between January 2003 and January 2008. During 5 years we treated 2,000 new patients with eczema. The majority of these children suffered from atopic dermatitis and were only patch tested when atopic dermatitis was refractory or when symptoms were suggestive of contact allergy.

2008 S. Karger AG, Basel 10188665/09/21820119$26.00/0 Fax +41 61 306 12 34 E-Mail karger@karger.ch www.karger.com Accessible online at: www.karger.com/drm

F.B. de Waard-van der Spek, MD, PhD Paediatric Dermatology Unit, Department of Dermatology Erasmus MC, PO Box 2040 NL3000 CA Rotterdam (The Netherlands) Tel. +31 10 703 6656, Fax +31 10 703 6707, E-Mail f.dewaard@erasmusmc.nl

Reasons for Patch Testing All patients with suspected ACD by history or localization or with uncontrolled or deteriorating atopic dermatitis were patch tested. Our criteria for patch testing were very strict. Patch Testing All patients were patch tested at our out-patient clinic at the Erasmus MC-Sophia Childrens Hospital. Patch tests were done using the TRUE test (panels 1 and 2), supplemented with tixocortol-17-pivalate, budesonide and 3 commonly used emollients (petrolatum 20% cetomacrogol cream, petrolatum 20% lanette cream, ung. leniens). Supplementary closed patch tests were undertaken if indicated by history, localization or positive results, using allergens from either Trolab Hermal or Chemotechnique diagnostics, Finn Chambers (10 mm) and Fixomull tape, applied in a standardized manner to the back. Concentration was not adjusted for the age of the patient. Chambers were removed on day 2. Reactions were read on 2 occasions after application (days 2 and 4) and were scored and interpreted according to the International Contact Dermatitis Research Group protocol [2].

Table 1. Numbers of patients with positive and negative reactions

subdivided according to indications Indication Atopic dermatitis Hand/foot eczema without atopy Others1 Total
1

Positive Negative reaction(s) reactions 22 9 9 40 25 9 5 39

Total number of patients 47 18 14 79

Localized eczema on the lower leg, perioral dermatitis, pruritus, suspected contact allergic reaction to several topical agents and adverse drug reactions.

Results

Reasons for patch testing were a refractory atopic dermatitis in 47 patients, localized hand and/or foot eczema without atopy in 18 patients, and others in 14 patients (localized eczema on the lower leg, perioral dermatitis, pruritus, suspected contact allergic reaction to several topical drugs and adverse drug reactions; table 1). Table 1 shows the results of patch tests subdivided according to indications. Of the 79 patients tested, 36 patients had 1 or more positive reactions to the allergens that were tested in all patients, and 4 patients had positive reaction(s) only to supplementary allergens. A total of 40 (51%) children consisting of 22 girls (aged 418 years) and 18 boys (aged 115 years) had 1 or more positive allergic patch test reactions. Of these 40 children, 22 (55%) had atopic dermatitis, 9 (23%) had hand or foot eczema without atopy, and 9 (23%) had other skin ailments. Five children in the age group 15 years and 35 children in the age group 6 years or older had 1 or more positive reactions. Table 2 shows the results of the TRUE test and the supplementary tests. Table 3 shows the indication for patch tests and the positive reactions in the age group 15 years. Nickel is the most common contact allergen in children younger than 18 years in the study population of our Paediatric Dermatology Unit. Of the 40 children with 1 or more positive allergic reactions, 17 (43%) had a positive reaction to nickel sulphate.
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Frequently used emollients showed a positive allergic patch test reaction in only a few cases. Two children had positive allergic reactions to the commercially available wool alcohols in the TRUE test. Four children had a positive patch test reaction to the emollient petrolatum 20% cetomacrogol cream and/or petrolatum 20% lanette cream: 1 child (with atopic dermatitis) showed a positive reaction to petrolatum 20% cetomacrogol cream, 1 child (with perioral dermatitis) showed a positive reaction to petrolatum 20% lanette cream, and 2 children (1 with atopic dermatitis and 1 with periocular dermatitis) showed positive reactions to both emollients. These reactions were not irritant reactions because when the results on day 2 and day 4 were compared, the characteristic crescendo reaction of contact allergy was observed. Other positive allergic patch test reactions in these children were found for sorbitan sesquioleate (SSO), cetomacrogol wax, sorbic acid and sorbitol. In atopic and non-atopic children with foot eczema, we tested material from their own shoes in addition to various known allergens. Six children showed an allergic patch test reaction to their own shoes, 3 of them were atopic. One child wore a blue leather case around his lower leg because of walking problems, which showed a positive allergic patch test reaction. Other positive allergic patch test reactions in these children were noted for potassium dichromate (3 children), p-tert-butylphenol formaldehyde resin (2 children), formaldehyde (1 child), p-phenylenediamine (PPD; 2 children), diethyl urea (1 child) and disperse red (1 child). Contact material from shinbone protectors showed a positive allergic patch test reaction in 5 children, all boys, 910 years old. Three of them had atopic dermatitis. All
de Waard-van der Spek/Oranje

Table 2. Number of patients with positive reactions to allergens in the TRUE test and in the supplementary tests, relevant or irrelevant to the actual skin problem and the indication

Allergen

Number of patients with positive reaction

Relevant to Atopic actual skin dermatitis (n = 22) problem 8 5 3 3 2 2 2 2 2 2 1 1 1 1 3 3 2 1 1 1 1 3 1 1 3 1 1 1 1 1 1 1 1 1 5 6 1 2 1 1 1 1 1 13 3 1 1 1 1 1 1 2 2 2 1 1 1 2 1 1 (20 min) 1 1 1 1 1 1 1 1 1 1 3 4 1 1

Other Hand/foot eczema without (n = 9) atopy (n = 9) 3 1 2 1 1 1 2 1 1 1 2 2 1 1 1 1 1 2 1 2 1 1 1 1 2 1 1 1 1 1 1 1 1 1 1

TRUE test Nickel sulphate 17 Potassium dichromate 5 p-tert-butylphenol formaldehyde resin 3 Formaldehyde 3 Fragrance mix 2 Quaternium-15 2 Cl+Me isothiazole 2 Thimerosal 3 p-Phenylenediamine 2 Thiuram mix 2 Wool alcohols 2 Mercapto mix 2 Carba mix 2 Cobalt dichloride 1 Colophony 1 Ethylenediamine dihydrochloride 1 Supplementary patch tests Petrolatum 20% cetomacrogol cream Petrolatum 20% lanette cream Sorbic acid 2% petr. Sorbitol 10% aq. Cetomacrogol wax Miconazole cream Miconazole/hydrocortisone cream Sorbitan sesquioleate 20% petr. Adaptic Cocamidopropylbetaine 1% aq. p-Aminoazobenzene 1% petr. Disperse red 1% petr. Cefotaxime Penicillin Roc Minesol 60 Xanthum gum Lip protector Labello Nivea body milk Capacho feet cream Shinbone protector Own shoes Blue leather case lower leg Toothpaste Diethyl urea 1% petr. ECG plaster (Meditrace) WNF plaster Chlorhexidine red Chlorhexidine colourless Petr. = Petrolatum; Aq. = aqueous. 3 3 2 (1 : 20 min) 1 1 1 1 3 1 1 3 1 1 1 1 1 1 1 1 1 5 6 1 2 1 1 1 1 1

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Table 3. The indication for patch tests and the positive reactions in the 5 children aged 15 years

Boy, 1 year old Boy, 3 years old

Skin reaction after several antibiotics Atopic dermatitis and resistant foot dermatitis

Cl+Me isothiazole, potassium dichromate, thimerosal, cefotaxime, penicillin Potassium dichromate, nickel sulphate, petrolatum 20% cetomacrogol cream, own shoes Chlorhexidine digluconate 0.5% in alcohol 70% (red), chlorhexidine digluconate 0.5% in alcohol 70% (colourless), p-aminoazobenzene 1% petrolatum, Meditrace plaster, WNF plaster Nickel sulphate, Roc Minesol, xanthum gum Carba mix, mercapto mix, sorbic acid 2% petrolatum (urticaria after 20 min)

Boy, 4 years old [3] Rather demarcated skin eruption after surgery Girl, 4 years old Girl, 5 years old Eczema after use of sunscreen Itchy, erythematous eruptions within several minutes after applying emollient

had eczema on the shins. The patient with a positive patch test to Adaptic non-adhering dressing also showed a positive reaction to SSO. The positive reactions were considered as clinically relevant to the present dermatitis if the patient described a cutaneous exposure to a product known to contain the allergen to which the patient reacted. Almost all positive reactions were relevant to the actual skin problem of the patient, except nickel [in 9 of 17 (53%) patients relevant], thimerosal (in all 3 patients not relevant for the actual problem), mercapto and carba mix in 1 of the 2 patients, and colophony in 1 patient not relevant to the present problem.

Discussion

This study supports the evidence that ACD is not uncommon in children with both atopic and non-atopic dermatitis. Epicutaneous patch testing in symptomatic children with dermatitis revealed positive reactions in up to 52% of the patients [4]. In asymptomatic healthy children, contact sensitization was found in 1320% of varying ages up to 18 years [5, 6]. Children as young as 6 months may be sensitized to contact allergens. From a paediatric population presenting for routine well-child care, 85 children aged 6 months to 5 years underwent epicutaneous patch testing. The prevalence of sensitization in this paediatric population was 24.5% [7]. In our study 5 children in the age group 15 years showed 1 or more positive reactions, whereas this was the case in 35 children in the age group of 6 years or older. ACD was suspected in all patch-tested children. In an earlier prospective open study in 33 children with atopic
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dermatitis (aged 515 years), Oranje et al. [8] reported 14 of 33 children with positive patch test reactions. Some reports stressed the necessity of investigating contact sensitization in infants, even in small babies. Seidenari et al. [9] reported a 12-month-old boy with atopic dermatitis and sensitization to nickel sulphate, which manifested itself as a sudden inexplicable hand and foot dyshidrosis. This child used to play with the metal rails of his hospital bed. This was the probable cause of sensitization, because changing the bed together with topical treatment induced a remission of the dermatitis [9]. Fisher [10] also reported ACD in early infancy. We encountered some of these cases too [A.P. Oranje, personal observations]. Fisher reported a 1-week-old infant with a strongly positive patch test reaction to epoxy resin, manifesting as band-like dermatitis above the wrist because of a vinyl band that was made of an epoxy resin. A 7month-old child with ACD from nickel-plated snaps on the back was mentioned, as well as ACD to ethylenediamine hydrochloride (a stabilizer) in early infancy [10]. Ethylenediamine-sensitive individuals must also avoid the use of antihistamines such as hydroxyzine chloride as these are ethylenediamine derivatives. Patients with asthma must avoid aminophylline, which is composed of theophylline and ethylenediamine. This study confirmed that ACD increases with age similar to that reported in various other studies [11, 12]. However, a decade ago the highest sensitization rate in one study in 670 children aged 6 months to 12 years was noted in children aged up to 3 years [13]. Of the 40 children with 1 or more positive allergic patch test reactions, 22 (55%) had atopic dermatitis, 9 (23%) had hand or foot eczema and 9 (23%) had other skin
de Waard-van der Spek/Oranje

ailments. Recently, Onder and Adisen [14] reported only 0.3% of the patients as having atopic dermatitis and positive allergic patch test reactions in their study in a paediatric population in Turkey. Goon and Goh [15] reported that 38% of the tested children and adolescents with positive patch test reactions were atopic. In our study, 22 of the 47 atopic children (47%) had positive patch test reactions corroborating the results reported in other studies [1, 12]. ACD is not rare in children with atopic dermatitis [11]. The damaged epidermal barrier encountered in patients with atopic dermatitis may play a role in the development of ACD in these patients. Children with atopic dermatitis are exposed to more sensitizers because of the used topical medications. However, in our study we did not find a high prevalence of positive patch test reactions to the used emollients or topical medications in children with atopic dermatitis. We always tested the used topical medications separately and found only 3 positive patch test reactions (2 for petrolatum 20% cetomacrogol cream and 1 for petrolatum 20% lanette cream) in patients with atopic dermatitis. Our results showed that nickel is the most common contact allergen in children younger than 18 years in the Dutch population of our Paediatric Dermatology Unit. Seventeen children (43%) showed a positive reaction to nickel sulphate, similar to that reported in earlier studies [1, 7, 11, 14, 15]. In a previous study in Rotterdam, the most positive patch test reactions in children aged 515 years were to nickel, cobalt and balsam of Peru [8]. However, in the study by Kohl et al. [16], metals (predominantly nickel) were listed only in third place, behind cosmetics and topical drugs as the cause of ACD in children. Even legislative measures have been implemented in order to reduce exposure to nickel. The increasing trend of body piercing in teenagers may partly explain the increasing reported rates of nickel allergy over the past years [1]. Many orthodontic appliances contain nickel, but their clinical relevance in nickel-allergic patients is unclear. Adverse reactions to orthodontic appliances in patients with nickel allergy have been observed, but are uncommon [17]. Kerosuo et al. [18] suggested that treatment with nickel-containing metallic orthodontic appliances before sensitization to nickel (ear-piercing) may reduce the frequency of nickel hypersensitivity. Kalimo et al. [19] reported in their study on 153 students that the development of nickel allergy was significantly associated with skin piercing. However, there were no significant differences in the development of nickel allergy among students who had permanent dental braces before or after skin piercing. Thus, they stated that orthodontic treatPatch Tests in Children with Suspected Allergic Contact Dermatitis

Table 4. Foot eczema in children with positive patch tests

Author Number of Age Positive patch test to allergen patients years 113 5 Rubber chemicals Potassium dichromate, cobalt chloride, colophony, balsam of Peru, p-tert-butylphenol formaldehyde resin Own shoes, potassium dichromate, p-tert-butylphenol formaldehyde resin, formaldehyde, PPD, diethyl urea, disperse red

Roul et al. [21] 8 Teixeira et al. 1 [22] Present study 6

314

ment may not lead to tolerance induction all the time, but sensitization due to permanent devices seems likely [19]. Nickel allergy is not a major hindrance for orthodontic treatment with fixed appliances in general but can sometimes cause adverse reactions in patients with presumed nickel allergy [20]. In atopic and non-atopic children with foot eczema, we found positive patch tests as shown in table 4 next to results from other studies. Contact dermatitis to shoes has not been extensively described in children. Nonetheless, if present, avoiding the shoes or allergens that have been identified is often sufficient to improve the symptoms. Two patients showed a positive patch test to PPD, and p-aminoazobenzene also showed a positive patch test in 3 patients. PPD is an aromatic arylamine and a wellknown and common cause of allergic contact dermatitis. It is used as an ingredient in permanent hair dyes, as photographic developing agent and as an intermediate in the manufacture of azo dyes, antioxidants and as an accelerator for rubber vulcanization. PPD is also sometimes added to henna to obtain a dark, blackish henna, and it is this substance that causes the majority of cases of contact dermatitis reported in subjects with black henna tattoos. Temporary tattoos painted with PPD-contaminated henna may have permanent consequences. The fashion of temporary henna tattoos in children should be discouraged because of the serious consequences of sensitization to PPD in the future. PPD may lead to ACD from hair dyes and cross-reactive chemical compounds such as azo dyes, sulphonamides, p-aminobenzoic acid sunscreens and local anaesthetics such as benzocaine or procaine [2325]. Three patients showed a relevant positive patch test to p-tert-butylphenol formaldehyde resin. Phenolformaldehyde resins, especially the p-tert-butylphenol formaldeDermatology 2009;218:119125

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hyde resin, are widely used in industry and in numerous materials such as glues, adhesives and inks for everyday use. The urticarial reaction to sorbic acid in the 5-year-old girl with atopic dermatitis could present non-immunological contact urticaria. Sorbic acid is well known as causing non-immunological urticaria. It is present naturally in several red fruits and also as a preservative in many cosmetic products and topical medicaments containing fatty acids or polyoxyethylene esters. One of our patients, a 9-year-old boy with perioral dermatitis, had positive allergic patch test reactions to sorbic acid, sorbitol, petrolatum 20% lanette cream, miconazole cream, miconazole/hydrocortisone cream and his toothpaste, which contained sorbitol. Contact dermatitis to sorbic acid is very rare in children. Systemic contact dermatitis to this preservative is also very rare, especially in children. A 1-year-old girl was reported with systemic contact dermatitis from alimentary ingestion of sorbic acid, presenting as itchy, scaly, erythematous lesions, confined to the fingertips of both hands. She often used moistened toilet tissues, which contained sorbic acid as an ingredient, to clean her hands [26]. Two children had positive patch test reactions to methylchloroisothiazolinone/methylisothiazolinone (MCI/ MI). MCI/MI has been widely used for the preservation of aqueous systems in cosmetics, toiletries and in various industrial applications. MCI/MI has a broad spectrum of activity against fungi and bacteria at very low concentrations. The allergic contact potential of MCI/MI has been known for many years. An 8-year-old child was reported with occupational ACD due to MCI/MI. He used beeswax containing MCI/MI for polishing furniture, helping his father. Children may be sensitized because it was widely used in skin care products and creams. The boy had already been diagnosed as being sensitized to MCI/ MI, because of exposure to toiletries, earlier in childhood [27]. In 811 Italian children with atopic dermatitis or other eczema, sensitization to preservatives was studied. 4.9% of the children reacted to MCI/MI, whereas !1% reacted to other preservatives [28]. Patch test reactions to SSO were positive in 3 children, all clinically relevant. In 2 children, the used emollient contained SSO as emulsifier. Recently, we reported a child with a positive patch test to Adaptic non-adhering dressing because of contact allergy to SSO together with 2 adults, in whom the recalcitrant wounds arose because of sensitization to Adaptic non-adhering dressings. Adaptic non-adhering dressing consists of liquid paraffin, polysorbate 80 (Tween 80), SSO (Arlacel C) and aqua purifi124
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cata [29]. Contact allergy to Adaptic non-adhering dressing because of SSO has been reported only incidentally. SSO is a mixture of the mono- and di-esters of sorbitol and its mono- and di-anhydrides with oleic acid. Sorbitan esters are oil-soluble, water-dispersible, non-ionic surfactants, which function as water-in-oil emulsifiers. SSO is present as an emulsifier in topical medicaments and cosmetics. It is also present as an emulsifier in fragrance mix and in composite mix. Patients may be falsely regarded as having an allergic reaction to fragrance mix and composite mix if they are not concomitantly patch tested with SSO [30]. It is important to realize that SSO is used as emulsifier in products formulated for treating skin lesions, also in the paediatric population. Recently, 6 other paediatric patients were reported with clinically relevant SSO contact allergy [31]. We did not find positive patch test reactions to the corticosteroid indicators tixocortol-17-pivalate and budesonide, or to the supplementary tested topical corticosteroids used by the patients. Corticosteroid contact allergy does not seem to explain an aggravation of the dermatitis during topical treatment with corticosteroids in a significant number of patients. This is similar to the results reported by Foti et al. [32]. ACD is common in children with both atopic and nonatopic dermatitis. Clayton et al. [11] observed no statistical difference in the relationship between the site of primary dermatosis and a positive patch test result. They stated that any child with persistent eczema should be referred for patch testing. The pattern of the presenting dermatitis in children should not determine referral for patch testing [11]. However, a suspect localization of skin lesions may be one of the indications for patch testing. Patch testing should be considered in any child with eczema or nonspecific dermatitis that is difficult to control. It is useful to test samples of own materials in addition to the commercially available allergens. Controls should also be tested in order to exclude possible toxic reactions. However, for practical reasons, we first chose to evaluate the severity of the reaction in time. We observed the characteristic crescendo reaction of contact allergy. After this observation we decided not to test controls because we did not want to risk active sensitization in (control) children. The documented rates of ACD in children are on the increase [33]. Sensitization to contact allergens begins in infancy and continues to be more common in older infants and young children. Infants, even neonates, may be sensitized [34]. ACD in childhood may also affect decisions regarding future occupations in adulthood. Therefore, it is very imde Waard-van der Spek/Oranje

portant that any contact allergy in a child is recognized and dealt with in time. However, there is a potential risk of active sensitization by patch testing. The same test concentrations as those used in adults should also be used in children [35]. However, Fisher [34] suggested the use of lower concentrations of some allergens in young children in order to avoid irritant reactions. In our opinion, children should be tested strictly based on the indication using a standardized protocol. We should also bear in mind that negative patch test results do not exclude contact dermatitis. We must constantly remain alert to the possibility of rare or new sensitizers. False-negative reactions have various causes, often a

missed allergen, which may be picked up by detailed questioning. Recognition of presenting signs and symptoms and appropriate patch testing are imperative when evaluating children with potential ACD. Patch testing is warranted in recalcitrant atopic dermatitis especially in children aged 5 years and older. Good information on preventing the development of ACD in children is useful for the caregivers. After all prevention is better than cure!

Acknowledgement
Dr. B. Tank is thanked for correcting the English.

References
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