Photoallergic contact dermatitis

 

An Goossens

Contact Allergy Unit

Department of Dermatology

Katholieke Universiteit Leuven

B-3000 Leuven, Belgium

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Photoallergic contact dermatitis is a classic T-cell-mediated or delayed-type hypersensitivity reaction of the skin in response to a photoallergen or photoantigen in a person who has been previously sensitized to the same chemical or one that cross-reacts with it.  The lesions, well demarcated and mostly symmetrical, generally occur on areas that are exposed to the light.  However, they may be distributed differently depending on the part of the body exposed or because of transfer from one part of the body to another.  Sometimes the original application site is not affected while an exposure to the sun produces a reaction on both exposed and non-exposed areas.  As with allergic contact dermatitis, the lesions usually clear when contact with the photoallergen ceases.  Occasionally, however, the patient may continue to develop lesions in the presence of sunlight even after removal of the photoallergen and may present recurrent transient or persistent light reactions (chronic actinic dermatitis).  Although photoallergic contact dermatitis is considered uncommon, many topical photoallergenic culprits have been reported in the literature, the most important of which are sunscreen agents and non-steroidal anti-inflammatory agents.

 

 

Key words: allergic photocontact dermatitis, clinical symptoms, non-steroidal anti-inflammatory agents, sunscreen agents, photoallergens.

 

 

 

 

 

Introduction

 

Both topically applied and systemically administered substances can produce photoallergic reactions.  As systemic reactions have been extensively reviewed in another article (1), we will focus here on photoallergic reactions induced by the topical contact of the skin with a chemical in the presence of, or followed by, exposure to UV or visible light.  Some of the more recently observed photoallergens or those producing peculiar clinical features will be discussed.  However, we do not intend to provide an exhaustive review here of all the photoallergens that have been reported.

 

Mechanisms

 

Photoallergic contact dermatitis is a classic T-cell-mediated or delayed-type hyper-sensitivity reaction of the skin in response to a photoallergen or photoantigen in a subject who has previously been sensitized to the same or a cross-reacting chemical.  The precise mechanism of the formation of a photoallergen by UV or visible light is poorly understood but two mechanisms have been proposed (2):

 

1)      A specific chromophore (a molecule able to absorb light) may be transduced into an excited unstable state.  As the molecule reverts to its ground state, the released energy might lead to conjugation with a carrier.

2)      A stable photoproduct is formed that serves as a hapten that conjugates with a carrier and thereby forms a complete antigen.

 

After a complete antigen is formed, the pathogenesis of a photoallergic contact dermatitis is essentially identical to that of allergic contact dermatitis: epidermal Langerhans cells process the antigen and present it - in association with class-II major histocompatibility complexes - in the draining lymph nodes to antigen-specific T-lymphocytes.  Cutaneous lesions will develop when activated T-cells circulate to the exposed areas of the skin and recognize the photoallergen (2).

For most of the photoallergens the action spectrum lies in the UVA range, but some elicit reactions in both the UVA and UVB range as is the case with diphenhydramine hydrochloride (3, 4) and non-steroidal anti-inflammatory agents (NSAIDs) (5).

The duration of the response to light irradiation after stopping the application of a known photoallergen is variable and depends on the photoallergen.  For sunscreens, for example, it is probably less than 4 days (6).  However, NSAIDs such as ketoprofen may cause subjects to react to sunlight up to several weeks after having stopped its local application (7, 8).  This is most probably due to retention of the molecule for up to at least 17 days (9) in the epidermis.

As with allergic contact dermatitis, avoiding the photoallergen usually clears the dermatitis.  Occasionally, even after withdrawal of the photoallergen, the patient may continue to develop dermatitis in the presence of sunlight and may present recurrent transient, i.e. up to several weeks or months, e.g. with thiourea derivatives (10) and ketoprofen (8, 11), or persistent light reactions (chronic actinic dermatitis), such as with ketoprofen (8, 11) and chlorproethazine (12).  The formation of endogenous photosensitizers might perhaps explain this phenomenon (13).

Sometimes contact allergic reactions are aggravated by light-exposure (photo-aggravation or photo-augmentation).  Examples of such allergens are thiourea (10), NSAIDs (see 14 for a review), including etofenamate (15), tosylamide/formaldehyde resin (16), and fragrances (17).  However, photoaggravation may sometimes be followed by transient (e.g. 8, 10) or persistent light reactions (8).

Moreover, persistent photosensitivity (chronic actinic dermatitis) may follow chronic contact allergy as is the case with some plants, e.g., Compositae (sesquiterpene lactones) (18, 19), fragrances and lichens (20).  This may also be the case with colophony (21) and ketoprofen (8, 11).

Cross-reactions between chemically related substances have been frequently reported: chlorproethazine cross-photoreacts with other phenothiazines (12).  Ketoprofen cross-photoreacts with oxybenzone, sulisobenzone, fenofibrate, tiaprofenic acid, piketoprofen (11), and unsubstituted benzophenone (11, 22), for which Bosca (23) had determined that photoallergy is indeed due to the benzophenone moiety of the cross-reacting chemicals involved.  Pigatto et al. (24) observed cross-reactions between ketoprofen and naproxen and between ibuprofen and naproxen in particular, as well as between ketoprofen and ibuproxam and cinnamic aldehyde.  They suggested that the ketonic group in the ketoprofen and cinnamic aldehyde molecules, and also in tiaprofenic acid after its conversion, could trigger the cross-reactions observed.  However, concomitant multiple sensitivities seem to be frequent in such patients (22) and could well offer a valid alternative explanation.  Moreover, associated photoallergic reactions between ketoprofen and molecules not having a benzophenone moiety, such as dibenzoylmethane derivatives, tetrachloro-salicylanilide and fentichlor (25), have also been reported.  We ourselves have observed associated reactions upon photopatch testing with suprofen and etofenamate (data on file).

 

Clinical features

The clinical symptoms of photoallergic contact dermatitis are those of an eczematous reaction with histopathological features identical to other forms of allergic contact dermatitis.  It may be acute, subacute, or chronic.  There are, of course, many similarities with phototoxic reactions, and clinical and histological features may help to differentiate between them (2).

Photoallergic contact dermatitis generally affects well-demarcated areas of the light-exposed areas: the face, neck, and V-area of the upper chest, the backs of the hands and forearms, and sometimes the legs.  A unilateral reaction may occur upon the application of a photoallergen to a particular body site and subsequent sun exposure or greater exposure of one body site (13).  The photoallergen may be transferred from one body site to another, for example, to the contra-lateral areas (8), or may be due to a cross-leg effect or to transfer by the hands (ectopic dermatitis)(le Coz, personal communication).  A particular distribution of the lesions may occasionally be a connubial photoallergic contact dermatitis (26, 27).

Furthermore, the original application site may not be affected while a subsequent sun exposure produces a reaction on exposed as well as non-exposed areas, as has been reported for ketoprofen (e.g. 8).

Photoallergic contact dermatitis may resemble an allergic airborne contact dermatitis (28), although a photo-induced dermatitis tends to spare the anatomically shadowed portions of the body such as the eyelids, the retro-auricular and submandibular regions, and those covered by hair.  Of course, "airborne" substances may have allergenic as well as both phototoxic and photoallergenic properties.  Occupation-induced airborne photoallergic dermatitis has been described for olaquindox (29), which cases may be followed by transient or persistent light reactions (30), the pesticides Maneb® and Fenitrothion® (31), as well as mancozeb and tetrachloroisophtalonitrile (Daconil®) (32).  A reaction to tetrachloro-isophtalonitrile may be followed by a persistent light reaction (32).

In addition to airborne dermatitis, also the topical application of contact allergens on exposed areas and chronic actinic dermatitis must be considered in the differential diagnosis, although the patients suffering from such diseases are at increased risk of developing photoallergy (33).  Moreover, certain other skin conditions like rosacea and lupus erythematosus may be photoaggravated.

Peculiar clinical features may sometimes occur, such as an erythema-multiforme-like eruption (11, 26, 34), leukomelanoderma ( 35), and a lichenoid photosensitive eruption (36) as may occur to Parthenium hysterophorus (already known as a possible cause of chronic actinic dermatitis and photocontact dermatitis).  Urticarial reactions and purpuric lesions (particularly on the lower legs) due to ketoprofen have also been described (Le Coz, personal communication).

Systemic reactions, including fever, rigors, diarrhea (37), and even abnormalities of liver function (38) have been reported in association with photocontact dermatitis.

 

The photoallergens

Although photoallergic contact dermatitis has been considered to be uncommon (33), the literature cites several topical substances that give rise to it.  Some substances may exceptionally have a photoallergenic effect as cadmium in tattoos (39), cinchocaine (40), certain NSAIDs such as fepradinol (41), flufenamic acid and etofenamate (42), Zovirax cream (43), and the sunscreen agent octyl triazone (44), but others do so frequently.   De Groot et al. (45) give a comprehensive list of topical photoallergens in drugs and cosmetics although not all of the cases reported have been critically reviewed (46).  Some occupational photoallergens have also been reported (47).

In the past, most photoallergic reactions resulted from the use of deodorant soaps containing halogenated salicylanilides and related compounds, and later on musk ambrette and 6-methylcoumarin in fragrances were identified as important photoallergens (46).  Nowadays, among the most frequently observed photoallergens are sunscreens containing benzophenones and dibenzoylmethane derivatives (33, 48-51).  However, in the south of Europe, but also in northern "sunny" regions, such as in Scotland (52) and Southern Sweden (53), and even in Belgium (data on file), photoallergic contact dermatitis due to topical application of the NSAID ketoprofen is increasingly being reported.  Photocontact dermatitis has also been attributed to suprofen and benzydamine (see 14 for a review).  Most of these molecules are also phototoxic and contact allergenic, in the latter case often associated with photo-aggravation (7, 8, 11).

Of course, the differences in composition of the standard set of photoallergens influence the frequency of the photopatch-test results obtained (51).

 

Conclusion

Photoallergic contact dermatitis has been regarded as rare.  Actually, the main photocontact allergens seem to be sunscreen agents and non-steroidal anti-inflammatory drugs (ketoprofen in particular).  However, in view of the misleading clinical features observed in some cases, the diversity of causal substances identified, and the low frequency with which photopatch testing is carried out in general, the occurrence of photoallergic contact dermatitis might well be underestimated.


References

 

1.       Ferguson J.  Photosensitivity due to drugs.  Photodermatol Photoimmunol Photomed 2002; 18: 262-269.

2.       Mang R, Krutmann J.  Mechanisms of phototoxic and photoallergic reactions.  In: Rycroft RJG, Menné T, Frosch PJ, Lepoittevin J-P (eds), Textbook of contact dermatitis, 3rd ed., Berlin: Springer, 2001; 134-143.

3.       Emmett EA.  Diphenhydramine photoallergy.  Arch Dermatol 1974; 110: 249-252.

4.       Yamada S, Tanaka M, Kawahara Y, Inada M, Ohata Y.  Photoallergic contact dermatitis due to diphenhydramine hydrochloride.  Contact Dermatitis 1998; 38: 282.

5.       Adamski H, Benkalfate L, Delaval Y, Ollivier I, Le Jean S, Toubel G, Le Hir-Garreau I, Chevrant-Breton.  Photodermatitis from non-steroidal anti-inflammatory drugs.  Contact  Dermatitis 1998; 38: 171-174.

6.       Buckley D A, Wayte J, O'Sullivan D, Murphy G M.  The duration of response to UVA irradiation after application of a known photoallergen.  Contact Dermatitis 1995; 33: 138-139.

7.       Le Coz CJ, El Aboubi S, Lefèbvre C, Heid E, Grosshans E.  Photoallergy from topical ketoprofen: a clinical, allergological and photobiological study.  Abstract,  Contact Dermatitis 2000; 42 (suppl): 47.

8.       Durieu C, Marguery M-C, Giordany-Labadie F, Journe F, Loche F, Bazex J.  Allergies de contact photoaggravées et photoallergies de contact au kétoprofène: 19 cas.  Ann Dermatol Venereol 2001; 128: 1020-1024.

9.       Sugiura M, Hayakawa R, Kato Y, Sugiura K, Hashimoto R.  4 cases of photocontact dermatitis due to ketoprofen.  Contact Dermatitis 2000; 43: 16-19.

10.     Dooms-Goossens A, Chrispeels MT, De Veylder H, Roelandts R, Willems L, Degreef.  Contact and photocontact sensitivity problems associated with thiourea and its derivatives: a review of the literature and case reports.  Br J Dermatol 1987; 116: 573-579.

11.     Le Coz CJ, El Aboubi S, Lefèbvre C, Heid E, Grosshans E.  Topical ketoprofen induces persistent and recurrent photosensitivity.  Abstract, Contact Dermatitis 2000; 42 (suppl): 46.

12.     Barbaud A, Collet E, Martin S, Granel F, Trechot P, Lambert D, Schmutz JL.  Contact sensitization to chlorproethazine can induce persistent light reaction and cross-photoreactions to other phenothiazines.  Contact Dermatitis 2001; 44: 373.

13.     White I.  Phototoxic and photoallergic reactions.  In: Rycroft RJG, Menné T, Frosch PJ, Lepoittevin J-P (eds).  Textbook of contact dermatitis. 3rd ed., Berlin: Springer, 2001; 367-379.

14.     Ophaswonge S, Maibach H.  Topical nonsteroidal antiinflammatory drugs: allergic and photoallergic contact dermatitis and phototoxicity.  Contact Dermatitis 1993; 29: 57-64.

15.     Sánchez-Pérez J, Sanz Sánchez T, García-Diez A.  Combined contact and photocontact allergic dermatitis to etofenamate in Flogoprofen gel.  Am J Contact Dermatitis 2001; 12: 215-216.

16.     Vilaplana J, Romaguera C.  Contact dermatitis from tosylamide/formaldehyde resin with  photosensitivity.  Contact Dermatitis 2000; 42: 311-312.

17.     Tani A, Hozumi H, Miyoshi H, Kanzaki T.  A case of photoallergic contact dermatitis to fragrances in aftershave cream.  Environ Dermatol 1999; 6: 105-109.

18.     Ross JS, Du Peloux Menagé H, Hawk LM, White IR.  Sesquiterpene lactone contact sensitivity: clinical patterns of cmpositae dermatitis and relationship to chronic actinic dermatitis?  Contact Dermatitis 1993; 29: 84-87.

19.     Kuno Y, Kawabe Y, Sakakibara S.  Allergic contact dermatitis associated with photosensitivity, from alantolactone in a chrysanthemum farmer.  Contact Dermatitis 1999; 40: 224-225.

20.     Lim HW, Morison WL, Kamide R, Buchness MR, Harris R, Soter NA.  Chronic actinic dermatitis: an analysis of 51 patients evaluated in the United States and Japan.  Arch Dermatol 1994; 130: 1284-1289.

21.     Kuno Y, Kato M.  Photosensitivity from colophony in a case of chronic actinic dermatitis associated with contact allergy from colophony.  Acta Derm Venereol 2001; 81: 442-443.

22.     Le Coz CJ, Bottlaender A, Scrivener J-N, Santinelli F, Cribier BJ, Heid E, Grosshans EM.  Photocontact dermatitis from ketoprofen and tiaprofenic acid: cross-reactivity study in  12 consecutive patients.  Contact Dermatitis 1998; 38: 245-252.

23.     Bosca F, Miranda MA, Carganico G, Mauleon D.  Photochemical and photobiological properties of ketoprofen associated with the benzophenone chromophore.  Photo-chemistry and Photobiology 1994; 60: 96-101.

24.     Pigatto P, Bigardi A, Legori A, Valsecchi R, Picardo M.  Cross-reactions in patch and photopatch testing with ketoprofen, thiaprofenic acid, and cinnamic aldehyde.  Am J Contact Dermatitis 1996; 7: 220-223.

25.     Martin S, Barbaud A, Pénétrat S, Tréchot P, Schmutz JL.  Existence of photoallergy between ketoprofen and molecules without any benzophenone moiety.  Abstract. Contact  Dermatitis 2002; 4 (suppl), 55.

26.     Mastrolonardo M, Loconsole F, Rantuccio F.  Conjugal allergic contact dermatitis from ketoprofen.  Contact Dermatitis 1994; 30: 110.

27.     Mirande-Romero A, González-López A, Esquivas JI, Bajo C, García-Muñoz M.  Ketoprofen-induced connubial photodermatitis.  Contact Dermatitis 1997; 37: 242.

28.     Dooms-Goossens AE, Debusschere KM, Gevers DM, Dupré KM, Degreef HJ, Loncke JP, Snauwaert JE.  Contact dermatitis caused by airborne agents.  J Am Acad Dermatol 1986; 15: 1-10.

29.     Francalanci S, Gola M, Giorginai S, Mucinelli A, Sertoli A.  Occupational photocontact dermatitis from Olaquindox.  Contact Dermatitis 1986; 15: 112-114.

30.     Schauder S, Schröder W, Geier J.  Olaquindox-induced airborne photoallergic dermatitis followed by transient or persistent light reactions in 15 pig breeders.  Contact Dermatitis 1996; 35: 344-354.

31.     Nakamura M, Arima Y, Nobuhara S, Miyachi Y.  Airborne photocontact dermatitis due to the pesticides maneb and fenitrothion.  Contact Dermatitis 1999; 40: 222-223.

32.     Matsushita S, Kanekura T, Saruwatari K, Kanzaki T.  Photoallergic contact dermatitis due to Daconil®.  Contact Dermatitis 1996; 35: 115-116.

33.     Darvay A, White IR, Rycroft RJG, Jones AB, Hawk JLM, McFadden JP.  Photoallergic contact dermatitis is uncommon.  Br J Dermatol 2001: 145: 597-601.

34.     Zhang X-M, Nakagawa M, Kawai K, Kawai K.  Erythema-multiforme-like eruption following photoallergic contact dermatitis from oxybenzone.  Contact Dermatitis 1998; 38: 43-44.

35.     Nabeya RT, Kojima T, Fujita M.  Photocontact dermatitis from ketoprofen with an unusual clinical feature.  Contact Dermatitis 1995; 32: 52-53.

36.     Verma KK, Sirka CS, Ramam M, Sharma VK.  Parthenium dermatitis presenting as photosensitive lichenoid eruption.  Contact Dermatitis 2002; 46: 286-289.

37.     de Groot AC, Van Der Walle HB, Jagtman BA.  Contact allergy to 4-isopropyl- dibenzoylmethane and 3-(4'-methylbenzilidene) camphor in the sunscreen Eusolex 8021.  Contact Dermatitis 1987; 16: 249-254.

38.     Parry EJ, Bilsland D, Morley WN.  Photocontact allergy to 4-tert.butyl-4'-methoxy-dibenzoylmethane (Parsol 1789).  Contact Dermatitis 1995; 32: 251-256.

39.     Yazdian-Tehrani H, Shibu MM,Carver NC.  Reaction in a red tattoo in the absence of mercury.  Br J Plast Surg 2001; 54: 555-556.

40.     Urrutia I, Jáuregui I, Gamboa P, González G, Antépara I.  Photocontact dermatitis from cinchocaine (dibucaine).  Contact Dermatitis 1997; 39: 139-140.

41.     Rodríguez Granados T, Piñeiro G, de la Torre C, Cruces Prado MJ.  Photoallergic contact dermatitis from fepradinol.  Contact Dermatitis 1998; 39: 194-195.

42.     Montoro J, Rodriguez-Serna M, Liñana JJ, Ferré MA, Sanchez-Motilla JM.  Photoallergic contact dermatitis due to flufenamic acid and etofenamate.  Contact Dermatitis 1997; 37: 139-140.

43.     Rodriguez-Serna M, Velasco M, Miquel J, De La Cuadra, Aliaga A.  Photoallergic contact dermatitis from Zovirax cream.  Contact Dermatitis 1999; 41: 54-55.

44.     Sommer S, Wilkinson SM, English JSC, Ferguson J.  Photallergic contact dermatitis from the sunscreen octyl triazone.  Contact Dermatitis 2002; 46: 304-305.

45.     de Groot AC, Weyland JW, Nater JP.  Unwanted effects of cosmetics and drugs used dermatology. 3rd.ed.  Amsterdam: Elsevier, 1994: 136-154.

46.     White IR.  Photopatch testing.  Chapter 27.  In: Rycroft RJG, Menné T, Frosch PJ, Lepoittevin J-P (eds).  Textbook of contact dermatitis, 3rd ed.,  Berlin: Springer, 2001: 527-537.

47.     DeLeo V.  Occupational phototoxicity and photoallergy.  In: Kanerva L, Elsner P, Wahlberg JE, Maibach HI (eds).  Handbook of Occupational Dermatology.  Berlin: Springer, 2000: 314-324.

48.     Gonçalo M, Ruas E, Figueiredo A, Gonçalo S.  Contact and photocontact sensitivity to sunscreens.  Contact Dermatitis 1995; 33: 278-280.

49.     Schauder S, Ippen H.  Contact and photocontact sensitivity to sunscreens.  Review of a 15-year experience and of the literature.  Contact Dermatitis 1997; 37: 221-232.

50.     Berne B, Ros A-M.  7 years experience of photopatch testing with sunscreen allergens in Sweden.  Contact Dermatitis 1998; 38: 61-64.

51.     Bakkum RSLA, Heule F.  Results of photopatch testing in Rotterdam during a 10-year period.  Br J Dermatol 2002; 146: 275-279.

52.     Horn HM, Humphreys F, Aldridge RD.  Contact dermatitis and prolonged photo-sensitivity induced by ketoprofen and associated with sensitivity to benzophenone-3.  Contact Dermatitis 1998; 38: 353-354.

53.     Hindsén M, Bruze M, Zimerson E. Fotoallergi mot ketoprofen i södra Sverige.  Abstract of paper presented at the Svenska Läkaresällskapets Riksstämma (27-29 November, 2002).  Program Sammanfattningar, p.149.