This study describes the case of a patient who developed symptoms of rhinoconjunctivitis on exposure to budgerigars and parrots. An IgE‐mediated allergy to budgerigar, parrot and pigeon antigens was demonstrated using both in‐vivo challenge tests (skin and nasal provocation tests) and in‐vitro investigations (radio‐allergo‐sorbent test, histamine release test). The study shows that the development of nasal disease can be associated with allergy to avian antigens. Copyrigh

Dieges, P.H.

Gerth van Wijk, R. (Roy)

Toorenenbergen, A.W. (Albert) van

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Clinical Allergy, 1987. Volume 17. pages 515 521Nasal allergy to avian antigensR. GERTH VAN WIJK. A. W. VAN TOORENENBERGEN* andP. H. DIEGESDepartment of Allergology and * Laboratory of Allergology (Department of ClinicalChemistry). University Hospital Dijkzigt Rotterdam, The Netherlands(Received in originat form 2 December 1986 and in revised form 3 April 1987;accepted for publication 6 April 1987}SummaryThis sludy deseribes the ease ofa patient who developed symptoms of rhinoeonjuncti-vitis on exposure to budgerigars and parrots. An IgE-medialed allergy to budgerigar,parrot and pigeon antigens was demonstrated using both in-vivo ehallenge tests (skinand nasal provoeation tests) and iti-ritro investigations (radio-allergo-sorbent test.histamine release test). The study shows that the development of nasal disease can beassoeiated with allergy to avian antigens.IntroduetionThe development of hypersensitivity pneumonitis in bird faneiers is well known. Thedisease was first described in pigeon breeders in 1965 by Reed et al. [1]. Exposure toother birds may also induee this disease [2-5]. Type HI and type IV allergic reactionsmay be involved [6], There is evidence that IgE-mediated mechanisms may also play arole in allergy to bird-derived materials [7 9]. Isolated nasal allergy to avian antigenshas rarely been reported. To our knowledge only Pelikan & Pelikan-Filipek [10] haveanalysed the nasal complaints in pigeon breeders.Subject and methodsMrsD. female. 47-years-old. had a hislory of perennial rhinoeonjunctivitis. Symptomsof running nose, sneezing and itching ofthe eyes had started 7 years previously and hadgradually become worse. She had chronic symptoms with acute aggrevation immedia-tely after contact with the budgerigar and the parrot, which she had been keeping for 8years outside the house. This exacerbation continued for about 24 hours. She had nosymptoms after contact with her pigeons. The history revealed no other provokingallergens. Other stimuli were non-specific (tobacco smoke, painty smell and fog). SheCorrespondence: R. Gerth van Wijk, Deparlment of Allergology. University Hospital Dijkzigl. DrMolcwiitcrplein 40. 3015 GD Rotlerdatn. The Netherlands,515516 R. Gerth van Wijk, A. W. van Toorenenbergen and P. H. DiegesTable I, Intradermal skin testsConcentration0-00025 0 0025 0 025 0-25 mg/ml (feather extract)Allergen 10-^ 10- ' 10-* 10-'' v/v (pigeon serum)Budgerigar feather + + + -I- -|- -i-Parrot feather + + + + + +Pigeon serum — + 4- + +4-Skin test response of patient D.. expressed according lo the grading system ofNorman [11). — Represents an erythema and weal of < 5 mm each: + reaction:erythema and weal of 5 10 mm each; 4- reaction: erythema of 11 20 mm andweal of 5-10 mm: +-t- reaction: erythema n!" 21 .10 mm and wcsil of 5 10 mm:-I- 4- 4-reaction: erythema of 31^0 mm and a weal of 10-15 mm or wilhpseudopods: + + + + reaction: erythema > 40 mm and weal > 15 mm or manypseud opods.had never experienced atopic dermatitis. No features of bronchial asthma orhypersensitivity pneumonitis were present. Spirometry. bronchial provocation withhistamine and a chest X-ray gave normal results. There was marked blood eosinophilia(0-673x10^ cells/litre).AllergensLyophilized budgerigar and parrot feather extracts and lyophilized pigeon serum wereobtained from Diephuis Laboratorium. Groningen, The Netherlands.Skin testsDilutions of budgerigar and feather extraets fO-25. 0025 and 0 0025 mg/ml) anddilutions of pigeon serum (10 \ 10 ''. 10 ^ and 10 *  v/v) were made using ettraetreconstituted in phosphate buffered saline (PBS) containing HSA 0 03% and phenol0-5%. Intradermal skin tests were performed and reactions were read after 20 minusing the grading system of standardized plus signs, devised by Norman [11].Nasal provocation testsLyophilized feather extract and serum were reconstituted with PBS containing HSA0 03% and benzalkonium chloride 0 5'>ii. After nasal provocation with 0 2 ml PBS ineach nostril, dilutions of parrot or budgerigar feather extract (from 0-025 to 2-5 mg/mlin ten-fold steps), pigeon serum (from 10 • to 10 - v/v in ten-fold steps) or histaminechloride (in dilutions of 0-25 and 0-5 mg/ml) were sprayed into each nostril using adeVilbiss atomizer connected to a pressure pump. The allergens were applied at 15-minintervals and histamine chloride at lO-min intervals. All tests were performed onseparate days.Total nasal airway resistance (NAR) was measured and calculated using a passiveanterior rhinomanometer (Heyer Parr) as described by Clement ct ai. [12]. Sneezeswere counted and secretion was collected as described by Borum [13],Nasal allergy to avian antigens 517800 p • ( 1 - 2 )* 600•41400• 7 ) .£ 200cc"^  0a>DI 2000, • {0-55)Before PBS 0-025 0-25 2-5 25provocotion iQ-5 ,Q-« iQ-j IQ-?mg feather extroct/mL buffer pigeon serum (v/v)Fig. 1. Increase in nasal resistance, expressed as percentage of the baseline value, induced by nasalprovocation wilh allergen extract in Mrs D, (•) and a non-aiopic control (O), Dose-response curves areconsiructed for budgerigar feather extract ( • • ) . parrot leaiherexiract ( • • ) and pigeon serum( • — • ) , When a measurable amount of secretion was produced, the amount in ml is included inparentheses.Total IgF and allergen-specific IgETotal IgE was determined using IgE RIA (Pharmacia, Uppsala, Sweden), according tothe manufacturer's instructions. Allergen-specific IgE was determined by a radio-allergo-sorbent test using agarose beads as allergen support. Bird allergens wereprepared and coupled to CNBr-aetivated Sepharose 4B as described previously [9].Precipitating anlibodiesPrecipitating antibodies against feather extract from budgerigar and parrots, andagainst serum from pigeons, were determined by double diffusion using the methoddescribed by Ouchterlony [14],Histamine release from washed leucocytesIneubation of washed leueocytes with allergen extracts (budgerigar feathers, parrotfeathers and pigeon serum) and assay of histamine released into the supernatant, wereperformed using Siraganian & Hook's method [15] as described previously [9].ResultsSkin testsIntradermal skin tests with extracts of house dust mites, pollens, animal danders andmoulds were negative. Mrs D showed immediate type skin reactions to bothbudgerigar and parrot feather extract and to pigeon serum (Table I). Non-specificeffeets ofthe extracts could be exeluded as three non-atopic controls showed no skinreactivity to the avian antigens.518 R. Gerth van Wijk. A. W. van Toorenenbergen and P. H. DiegesTable 2. IgE against avian antigensBudgerigar Parrot Pigeon TotalIgEFeathersSerum 17Serum15Feathers25Serum21Feathers5Scrum15IU/ml500Serum from Mrs D, tested for the presence o!" IgE to budgerigar, piirrot andpigeon feathers and serum. Results are expressed as binding of '-^I anti-IgE.Table 3. Test for non-specific binding to bird antigens123456BudgerigarFeathers11Serum00ParrotFeathers Serum0 03 1PigeonFeathers Serum0 00 0TotalIU/ml35513503655500540700Six sera with various total IgE levels were incubated with Sepharose-coupled avian antigens.Table 4. IgF. against parrot antigensPatientA,W.Ro.Ry.ParrotFeathers9152427Serum01432Total IgEIU/ml14004504000340Sera from four patients showing speci-fic IgE to parrot feathers and sera. Theresults are expressed as binding of '-"^  !-anti-IgE,Na.sal allergy to avian antigens 51950c[Mrs D.J L10"^ 10"'' 10"^ 10^' 10"' 0mg feather extract /mL buffer pigeon serum (v/^)Fig. 2, Histamine release from leticocytes from Mrs D, (•) and from a non-atopic control (O) on incubationwith budgerigar feather extract ( • • ) , parrot feather extract ( • • ) and pigeon serum ( • • ) .Nasal provocation testsA marked increase of NAR was seen after provocation with avian antigens (Fig. I).This nasal response could not be induced in a non-atopic control. Indicating that thebird-derived materials that we used had no irritating effect on the nose. Histaminechloride (0-25 mg/ml) caused an increase in NAR of 175% ofthe basehne value andproduced 0-75 ml of secretion.Total IgE and allergen-specific IgESerum obtained from the patient was tested for the occurrence of total and allergen-specific IgE. IgE against all feather extracts and the corresponding bird sera was found(Table 2).In order to exclude non-specific binding to bird antigens, control studies werecarried out by testing sera with total IgE levels between 300 IU/ml and 1300 IU/ml, Abinding of 0-3% was found (Table 3), Control studies of the budgerigar feather RASTare described elsewhere [9].We looked for patient sera with IgE binding to parrot antigens to find out whetherthis was an isolated phenomenon. In patient sera sent from other departments in theperiod 1984-1986 we found four sera containing IgE against parrot antigens (Table 4).Precipitating antibodiesIn Ouchterlony tests with serum from Mrs D., which was incubated with extracts offaeces or feathers or with serum from budgerigar, parrot or pigeon, there were either noprecipitates or they were only weak.Histamine relea.se from washed leucocytesThe histamine release test showed that leucocytes obtained from the patient releasedhistamine after incubation with budgerigar or parrot feather extract or pigeon serum,whereas a normal donor showed no release on exposure to these avian antigens(Fig. 2).520 R. Gerth van Wijk, A. W. van Toorenenbergen and P. H. DiegesDiscussionIsolated nasal allergy to bird-derived antigens is imcommon. The liieraiure on allergyto avian antigens has focused on the development of lung disease [17], especially onhypersensitivity pneumonitis [I 5], Pelikan & Pelikan-Filipek [10] recorded a late nasalresponse to pigeon dropping challenge in 53"o of pigeon breeders with nasalcomplaints. Based on the occurrence of precipitating IgG antibodies, general malaise,increased body temperature and a rise in white blood count, they suggested that a typeIII hypersensitivity reaction was involved.The existence of IgE-mediated allergy has been established for budgerigars [7,9],canaries [9] and pigeons [8]. Type I allergy to parrot antigens seems to be uncommon,as it is only recently that a patient with an allergy to parrots and also egg yolk has beendescribed [16]. The diagnosis ofthe allergy to the parrots was established by hisloryand by RAST.In this report we have demonstrated IgE against bird-derived material from severalspecies. The findings ofa recent study [9] suggest that budgerigar and canary featherextracts contain more different IgE binding antigens than the corresponding bird sera,asonly patient sera containing high levelsof IgE against bird feather extract read, withbird serum. This is probably also true for parrot antigens, as all patient sera in thisstudy (Tables 2 and 4) showed IgE binding in the parrot feather RAST that was higherthan, or equal to, the corresponding serum RAST. However, the binding of IgE topigeon feathers was less than the binding to pigeon serum. A possible explanationcould be that a cross-reactivity exists between pigeon serum and other bird sera. It Isalso possible thai we did not use an optimal allergen concentration in the pigeonfeather RAST.In the nasal provoeation test., pigeon serum induced a significant nasal response(increase of NAR > 100%) in a concentration 10000 times higher than the concentra-tion needed for a I + skin reaction. The concentration of budgerigar feather extractneeded to elicit a nasal response was 100 times the concentration needed fora 1+ skinreaction, while for parrol feather extract the concentration needed was equal to thatfor a I -f- skin reaction. This suggests that the sensitivity to pigeon antigen in the targetorgan, the nose, was lower than the nasal sensitivity to budgerigar and parrot antigens,which in fact corresponds with the patient's history.In the nasal provocation tesl with hisiamine, Mrs D. reacted by producing aconsiderable amount of secretion when provoked with a low dose (0 25 mg/ml). Wereported in a recent study that healthy non-atopic subjects do not show any nasalresponse after application of this concentration [17]. This suggests the occurrence ofanon-specific nasal reactivity. Evidence for a relation between allergy and nasalhyperreactivity has been produced by Borum [18], who reported an increase inreactivity to histamine and methacholine in pollinosis patients during the pollensea .son.We conclude that rhinitis in bird fanciers can be associated with an IgE-mediatedallergy to bird antigens.References! Reed CE. Sosmon AJ. Barec RA. Pigeon breeder's lung. J Am Med Assoc I%5; 193:261 5.2 Korn DS. Florman AL. Gribet? I, Rcturrenl pneumonitis with hypersensitivity to hen litter. J .Am MeitAssoc 1968; 205:44 5,3 Boyer RS. Klock I.E. Schmidt CD cfu/. Hypersensitivity lung disease in the turkey-raising industr>. AmRev Respir Dis 1974, 109:630-5,Na.sal allergy to avian antigens 5214 Cunningham AL. Fink JN, Schlucter DP. Hypersensitivity pneumonitis due to droves. Pediatrics 1976;58:436-42.5 Hargreave FE, Pepys J, Longbottom JL, Wraith DB. Bird breeder s (fanciers) lung. Lancet 1966; i:4459.6 Richardson HB. Hypersensitivity pneumonitis—pathology and pathogenesis. Clin Rev Allergy 1983;1:464 86,7 Faux JA, Wide C. Hargreave FE. Longbottom JL. Pepys J. Immunological aspects of respiratory allergyin budgerigar {Melopsittacus undulatus) fanciers, Clin Allergy 1971; 1:149-58.8 Hbner H. Kraft O. Goct/ M ct at. Nachwcis von IgE Antikorpcrn gcgen Taubenserum und TaubenkotKomponenten mitlels RAST, In: Kolner RAST Symposion 3:161-5 (Grossc, Berlin. 1981),9 van Toorenenbergen AW. Gerth van Wijk R, van Dooremalen G. Dieges PH. Immunoglobulin Eantibodies against budgerigar and canary feathers. Int Arch Allergy Appl Immunol 1985; 77:433-7,10 Pelikan Z. Pelikan-Filipek M. A new disease: a nasai form of pigeon breeder's disease. Allergy 1983;38:309 18.It Norman PS. Skin testing. In: Rose NR. Friedman H. eds. Manual of clinical immunology. 2nd edn.Washington: Am Soc for Microbiology, 1980:789 93,12 Clement PAR. van Dishoeck EA. vd Wai RJ. Stoop AP. Hoeck GT, Van Strik R. The nose provocationand the passive anterior rhinomanometry (P.A,R,1 Acta oto-rhlnolaryngol Beig 1978; 32:56-63,13 Borum P, Nasal melacholine challenge. J Allergy Clin Immunol 1979; 63:253-7,14 Ouchterlony D, Antigen antibody reactions in gels; types of reactions in coordinated systems ofdiffusion. Acta Path Microbiol Scand 1959; 32:231^0.15 Siraganian RP, Hook WA, Histaminereleaseandassay methods for the study of human allergy. In: RoseN R. Friedman H, eds. Manual of clinical immunology 2nd edn. Washington: Am Soc for Microbiology,1980:808 21.16 de Maat-Bleeker F. Van Dijk AG. Berrens L. Allergy to egg yolk possibly induced by sensitization to birdserum antigens, Ann Allergy 1985; 54:245 8.17 Gerth van Wijk R. Dieges PH, Comparison of nasal response to histamine. methacholine andphenlolamine in allergic rhinitis patients and controls, Clin Allergy 1987; 17: 563-570,18 Borum P. Nasal reactivity in rhinitis. Fur J Respir Dis 1983; 64 {suppl 128): 65 71,

Nasal allergy to avian antigens

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