pissn: 2288-42 eissn: 2288-41 3(5):358-364, September 215 http://dx.doi.org/1.4168/aard.215.3.5.358 ORIGINAL ARTICLE 민들레화분항원의교차반응과주요알레르겐에대한 IgE 결합성분의규명 김지혜 1, 윤문경 1, 김미애 2, 신유섭 1, 예영민 1, 박해심 1 1 아주대학교의과대학알레르기내과학교실, 2 차의과학대학교분당차병원호흡기 알레르기내과 Cross-allergenicity between dandelion and major weed pollens Ji Hye Kim 1, Moon-Kyung Yoon 1, Mi-Ae Kim 2, Yoo-Seob Shin 1, Young Min Ye 1, Hae-Sim Park 1 1 Department of Allergy and Clinical Immunology, Ajou University Hospital, Suwon; 2 Department of Pulmonology-Allergy, CHA Bundang Medical Center, CHA University, Seongnam, Korea Purpose: The prevalence of pollinosis is increasing, and it is expected to increase further with climate change. Mugwort and ragweed pollens are well known as prevalent allergenic weed pollens in Korea. However, the clinical significance of dandelion pollen as an inhalant allergen has not yet been studied. The purpose of this study was to evaluate the clinical significance and cross-allergenicity between dandelion and major weed pollens. Methods: Ninety-seven patients with allergic rhinitis and asthma or with allergic rhinitis alone who were sensitized to dandelion pollens on skin prick tests (allergen/histamine ratio > 3) were enrolled between December, 212 and November, 213. Serum specific IgE levels to dandelion pollen extracts were measured by using enzyme-linked immunosorbent assay (ELISA). ELISA inhibition tests were performed to evaluate cross allergenecity with other weed pollens. Results: When the positive cutoff value for serum specific IgE was set at the mean ± 3 standard deviation of absorbance values, 52 patients (53.6%) had a high serum specific IgE antibody level. ELISA inhibition tests showed significant inhibitions with serial addition of dandelion pollen extracts, and 5 different inhibition patterns were noted with addition of 4 weed pollen extracts: significant inhibitions with pollens of mugwort, ragweed, chenopodium and Hop J (25%, 13 of 52), inhibitions with pollens of mugwort, ragweed and chenopodium (17.3%, 9 of 52), inhibitions with 2 pollens of mugwort and ragweed (32.6%, 17 of 52), inhibitions with mugwort pollen (21.1%, 11 of 52), and inhibitions with dandelion pollen alone (4%, 2 of 52). Conclusion: These findings suggest that dandelion pollen may be a causative inhalant allergen to induce pollinosis in the autumn season. Cross-allergenicity with other weed pollens showed individual differences; most patients had cross-reactivity with mugwort, ragweed, and chenopodium pollens, while some with Hop J pollen. Few patients were sensitized to dandelion pollen alone. (Allergy Asthma Respir Dis 215;3:358-364) Keywords: Taraxacum officinale, Cross-allergenicity, Pollinosis 서론꽃가루병은꽃가루가원인알레르겐으로작용하여알레르기비염, 천식, 결막염및아토피피부염을일으키는질환으로국내유병률은지속적으로증가하고있으며, 향후지구온난화및기후변화와함께점차증가할것으로예상된다. 1,2) 우리나라에는가을철꽃 가루병의주요원인꽃가루로잡초꽃가루가알려져있으며, 여기에는돼지풀 (ragweed), 쑥 (mugwort), 환삼덩굴 (Humulus japonicus, Japanese hop) 꽃가루가잘알려져있다. 1,3) 돼지풀과쑥꽃가루와같은잡초꽃가루는그발생량은적으나강력한알레르겐으로작용할수있어꽃가루병환자에서주의해야할식물이다. 4) 반면민들레꽃가루는충매화로, 명아주, 쑥꽃가루와함께국화 Correspondence to: Hae-Sim Park http://orcid.org/-3-2614-33 Department of Allergy and Clinical Immunology, Ajou University Hospital, 164 World cup-ro, Yeongtong-gu, Suwon 16499, Korea 215 The Korean Academy of Pediatric Allergy and Respiratory Disease Tel: +92-31-219-5196, Fax: +82-31-219-5154, E-mail: hspark@ajou.ac.kr The Korean Academy of Asthma, Allergy and Clinical Immunology This study was supported by a grant from the Korean Health Technology R&D Project funded by the This is an Open Access article distributed under the terms of the Creative Ministry of Health & Welfare, ROK (H14C2628). Commons Attribution Non-Commercial License Received: July 3, 215 Revised: July 22, 215 Accepted: August 5, 215 (http://creativecommons.org/licenses/by-nc/3./). 358 http://www.aard.or.kr
김지혜외 민들레화분항원의교차반응과주요알레르겐 과에속한다. 4) 대부분의국내알레르기클리닉에서시행하는알레르기피부반응검사항원패널에민들레꽃가루항원이포함되어있으나국내꽃가루력에민들레꽃가루의분포및계절적변화에대한보고가없고, 알레르기환자에서민들레꽃가루항원의임상적인의의에대한국내연구의보고가적다. 1) 한편유럽의보고에따르면, 민들레꽃가루추출액에의한감작률은접촉성알레르기환자에서.7% 1.4% 로낮고, 화훼전문가와같이직업적인노출이있는경우에는 4.5% 14% 로높다. 5) 이연구에서는민들레꽃가루의임상적유용성을평가하기위하여알레르기피부반응시험상민들레꽃가루에강양성반응을나타낸알레르기비염환자들의특이 IgE 항체를측정하고, IgE 결합성분과쑥, 돼지풀, 환삼덩굴꽃가루와의교차항원성을확인하였다. 대상및방법 1. 재료 1) 연구대상 212년 12월부터 213년 11월까지아주대학교병원알레르기내과를내원한환자중에서, 천식유무와관계없이알레르기비염으로진단된환자중에알레르기피부반응시험을시행하여민들레꽃가루에대한알레르겐 / 히스타민 (allergen/histamine, A/H) 비가 3 이상을나타낸환자 97명을대상으로하였다. 대상환자들의혈청은 8 C의냉동고에보관후실험에사용하였다. 2) 민들레및잡초꽃가루추출민들레꽃가루는 Taraxacum officinale (Allergon, ThermoFisher Scientific, Uppsala, Sweden), 돼지풀꽃가루는 Ambrosia artemisiifolia (Allergon), 쑥꽃가루는 Artemisia vulgaris (Allergon), 명아주꽃가루는 Chenopodium album (Allergon) 꽃가루를구입하여사용하였다. 환삼덩굴꽃가루는직접수원지역에서채집하여제조한항원 6) 을이용하여, 이전보고된방법과동일하게추출액을제조하였다. 7) 간략히기술하면, 각꽃가루 1 g을 phosphate buffered saline (PBS) 에넣고추출하고그추출액을원심분리한후,.45-μm filter를이용하여분리하였다. 분리된꽃가루항원내단백질정량은 Bradford assay으로, 단백띠는 sodium dodecyl sulphate-polyacrylamide gel electrophoresis (SDS-PAGE) 로확인하였다. 2. 방법 1) ELISA를이용한혈청내민들레항원에대한특이 IgE 항체치측정실험을위하여민들레꽃가루항원을 coating buffer (.1M carbornate-bicarbonate buffer, ph 9.6; Sigma-Aldrich Co., St. Louis, MO, USA) 에 5 μg/ml 농도로희석하여 96-well microplate (Corning, New York, NY, USA) 에 4 C에서 16시간동안반응시켰다. 다음날세척액 (.5% Tween-2 in PBS, ph 7.) 으로 3회세척후, 차단용액 (1% fatal bovine serum in PBS) 으로실온에서 2시간반응시킨후 3회세척하였다. Biotin-labeled goat antihuman IgE 항체 (Vector Laboratories Inc., Burlingame, CA, USA) 1:1, vol/vol 을 well당 1 μl씩넣고 1시간동안반응시킨후 3회세척하였다. 여기에 streptavidine-peroxidase (Sigma Co.) 1:1, vol/vol 을 well 당 1 μl씩넣고 3분간작용시킨후 3회세척하였다. 발색제 (3, 3, 5, 5-tetramethylbenzoet one tablet, phosphate citrate buffer 1 ml, 3% H 2O 2 2 μl) 를 well당 1 μl씩넣고상온에서 15분간발색후 2NH 2SO4 4 로발색을중지시키고, plate reader를이용하여 45 nm에서흡광도 (optical density) 를측정하였고, 정상대조군의평균값에 3배의표준편차를더하여 cutoff치 (253.33) 이상인경우양성반응으로간주하였다. 2) 민들레항원을이용한 IgE-ELISA 억제시험 5 µg/ml 농도의민들레꽃가루항원을 96-well microplate (Corning) 에각 well당 1 µl씩넣고 4 C에서 12시간이상반응시켰다. 혈청에서 ImmunoCAP (ThermoFisher Scientific) 으로측정한쑥꽃가루와돼지풀꽃가루에대한특이 IgE가모두 1 ku/l를초과하는혈청에억제제로민들레꽃가루항원을각각, 1, 1, 1 µg/ml씩추가하여 4 C에서 12시간이상반응시켰다. 비특이적결합을방지하기위해 1% PBS-Tween 2으로 3회세척후꽃가루항원을반응시킨환자의혈청을 well당 5 µl씩넣어상온에서 2시간반응시킨후, 상기기술한 ELISA법과동일한방법으로민들레꽃가루항원에결합하는특이 IgE 항체치를측정하였다. 특이 IgE 항체결합의억제도 (%) 는 ([ 대조군의흡광도 억제제가포함된 sample의흡광도 ]/ 대조군의흡광도 ) 에 1을곱한값으로정하였다. 3) 3) SDS-PAGE에의한민들레항원내단백질의확인민들레꽃가루항원을 sample buffer (.54M tris ph 6.8, glycerol, 1% SDS,.5% bromophenol blue, 2.5% ß-mercaptoethanol) 에희석하여 5분간가열하였다. 표지자와각각의항원을 4% 2% Trisglycerine gel (Novex, Invitrogen, San Diego, CA, USA) 에서 12 V, 2시간동안전기영동하여각각의항원단백띠를분리하였다. 4) IgE-immunoblot 방법을통한민들레꽃가루항원내 IgE와결합하는성분분석민들레의꽃가루항원추출액에서 SDS-PAGE 법으로항원단백을분리한후, 단백질을 poly-vinyl difluoride membrane (PVDF membrane, Millipore Co., Bedford, MA, USA) 에전이시켰다. 단백질이전이된각각의 PVDF membrane 에환자와대조군의혈청 1 ml을 2시간동안처리한후 Tris-buffer saline (TBST) 로 4회세척 http://dx.doi.org/1.4168/aard.215.3.5.358 359
Kim JH, et al. Allergenicity of dandelion pollen Table 1. Clinical characteristics of the study subjects (n= 97) Characteristic Value Age (yr) 34.67± 16.43 Male sex 49 (51) AR 97 (1) AR combined with BA 21 (21.6) Total IgE (IU/L)* 659.9± 813.7 Atopy 97 (1) Values are presented as mean± standard deviation or number (%). AR, allergic rhinitis; BA, bronchial asthma. *Total IgE levels are presented as geometric mean± geometric standard deviation. Atopy was defined as having more than 1 positive response to common inhalant allergens (i.e., tree mixture, grass mixture, mugwort, ragweed, cat fur, dog fur, Dermatophagoides pteronyssinus, Dermatophagoides farina, and Alternaria alternata) on the skin prick test. Specific lge to dandelion pollen extract (O. D. X 1,) 3, 2, 1, 하였다. Biotinylated antihuman IgE 항체 (Vector Laboratories Inc.) 를 1% fetal bovine serum-phosphate buffered saline을이용하여 1:1, vol/vol로희석하여상온에서 1시간작용시켰다. 이후 TBST로 3회세척한후각각의 membrane에 1X AP color development buffer와 AP conjugate substrate kit (Bio-Rad laboratories Inc., Hercules, CA, USA) 의혼합액을넣어단백띠가나타날때까지반응시켰다. 결과 1. 환자군의임상적특성민들레에대한 A/H 비가 3 이상인환자는총 97명이었다. 환자들의임상적특성은 Table 1과같으며, 모두알레르기비염환자였다. 2. 혈청특이 IgE 항체측정 ELISA 및 ELISA 억제시험민들레에대한 A/H 비가 3 이상인환자총 97명에서민들레꽃가루에대한특이 IgE 항체치측정을위한 ELISA 결과중 52명 (53%) 에서양성반응이확인되었다 (Fig. 1). 특이 IgE 양성인환자의혈청을이용하여 IgE ELISA 억제시험을시행하였고, 모두민들레항원에유의한반응이나타났다. 명아주, 쑥, 돼지풀, 환삼덩굴꽃가루항원에의해다양한억제반응이관찰되었고 5가지양상으로구분할수있었다. 억제농도 1 µg/ml에서 (1) 쑥, 돼지풀, 명아주, 환삼덩굴항원에모두억제된군 (A군, 13명 [25%], 5% 억제농도, 73% 87%), (2) 쑥, 돼지풀, 명아주항원에의해억제된군 (B군, 9명 [17.3%], 5% 억제농도, 52% 91%), (3) 쑥과돼지풀혹은쑥과명아주꽃가루에의해억제된군 (C군, 17명 [32.6%], 5% 억제농도, 51% 94%), (4) 쑥항원에만억제된군 (D군, 11명 [21.1%], 5% 억제농도, 52% 86%), 그리고 (5) 민들레항원에만단독으로억제된군 (E군, 2명 [4%], 5% 억제농도, 65% 92%) 을관찰하였다 (Fig. 2). 3. SDS-PAGE 법을이용한민들레꽃가루항원내단백띠확인 민들레꽃가루항원내단백띠는 7 개 (12 kda, 13 kda, 14 kda, 17 kda, 24 kda, 39 kda, 7 kda) 가관찰되었다 (Fig. 3). 4. IgE immunoblot 검사를이용한민들레항원내 IgE 결합 성분 Patients (n=97) SDS-PAGE 를통해확인한단백띠를토대로 IgE immunoblot 검 사를분석하여, 5 개의 IgE 와결합하는알레르겐성분 (12 kda, 14 kda, 17 kda, 24 kda, 39 kda) 을찾을수있었다 (Fig. 4). 대상환자 중 5% 이상에서나타나는 IgE 결합단백대를주요알레르겐 (major allergen) 으로정의하였을때, 59.1% (13 명 ) 의 IgE 항체와결합한 단백대 24 kda 을주요알레르겐으로정의할수있었다 (Fig. 5). 또 한 5 개군간에서결합양상의뚜렷한차이는관찰되지않았다. 고찰 Normal control (n=44) Fig. 1. Detection of serum specific IgE antibodies to dandelion pollen extracts by enzyme-linked immunosorbent assay in sera from 97 allergic rhinitis patients ( ) and 44 normal controls ( ). 국화과 (Compositae family) 에속하는대표적인잡초꽃가루에 는쑥꽃가루가있으며, 이는동일한계절에날리는돼지풀, 환삼덩 굴꽃가루와함께국내뿐만아니라환경이유사한중국, 일본등동 북아시아지역과북부유럽에서계절성알레르기질환과꽃가루병 을유발하는주요항원이다. 다양한연구에의하면가을철계절성 알레르기비염을유발하는잡초꽃가루에대한감작률은점차증가 하는추세이며, 두개이상의꽃가루에중복감작되어있는경우도 19.3% 로알려져있으며 6-8) Lee 등 9) 은감작률이증가하고있는꽃가 루의종류를쑥꽃가루, 돼지풀꽃가루및환삼덩굴꽃가루등이라 36 http://dx.doi.org/1.4168/aard.215.3.5.358
김지혜외 민들레화분항원의교차반응과주요알레르겐 1 1 1 8 8 8 6 4 2 6 4 2 6 4 2 1 1 1 Concentration of inhibitors (μg) 1 1 1 1 1 1 A Concentration of inhibitors (μg) B Concentration of inhibitors (μg) C 1 1 8 8 6 4 2 6 4 2 Dandelion Calbum Mugwort Ragweed Hop J 1 1 1 Concentration of inhibitors (μg) D 1 1 1 Concentration of inhibitors (μg) E Fig. 2. IgE-ELISA inhibition results for dandelion pollen extracts by serial addition of dandelion, mugwort, ragweed, Chenopodium album, and Japanese hop pollen extracts. (A) inhibition with 4 weed pollens; (B) inhibition with 3 weed pollens, including mugwort, ragweed, and C. album pollen; (C) inhibition with 2 weed pollens, including mugwort and ragweed pollens; (D) inhibition with mugwort pollen; and (E) inhibition with dandelion pollen alone. ELISA, enzyme-linked immunosorbent assay. 고보고하였다. 민들레꽃가루는쑥꽃가루와함께국화과에속하는데그임상적의의가잘알려져있지않다. 민들레꽃가루와알레르기질환과의관련성에대한국외보고는대부분직업성알레르기질환으로접촉성피부염에대한보고가있고 1-12) 건강보조제로민들레꽃가루항원을포함하고있는벌꽃가루 (bee pollen) 복용후발생한급성알레르기반응에대한국내외보고도있다. 13-15) 이처럼현재까지민들레꽃가루와알레르기질환과의관련성에대한보고는상대적으로드물고, 특히호흡기알레르기와민들레꽃가루의관련성에대한국내보고가없기때문에민들레꽃가루의임상적유용성을평가하였다. 대만에서보고한결과에따르면 419명의알레르기비염환자를분석한결과민들레꽃가루항원이원인인경우는 7명 (1.7%) 이었다. 16) 국내의한연구 7) 에서알레르기비염으로진단된환자에대해 전연령에걸쳐분석한결과민들레꽃가루항원에대한감작률은 3.% 13.4% 였고, 또다른연구 17) 에서피부반응검사상민들레꽃가루항원에감작되어있는환자가 8.5% 였다. 1만명을대상으로흡입항원감작률을조사한연구에서는 3 17세의비교적젊은연령에서가장많이감작되어있는 4개흡입항원중하나가민들레꽃가루항원이었다. 18) 본연구의결과피부반응검사상민들레꽃가루항원에양성인 97명중 54.6% 에서혈청내특이 IgE 항체가증가되어있었다. 피부반응시험단독으로양성인환자가 3명있었고민들레항원에만단독으로억제반응이관찰된환자도 2명이있었다. 이는, 국내호흡기알레르기환자에서도일부환자에서민들레꽃가루항원이가을철흡입알레르겐으로작용할가능성이있다는것을의미한다. 기후변화에따른꽃가루병의증가현상, 특히잡초꽃가루에의한감작률증가가관찰되고있어 19,2) 가을철잡초꽃가루 http://dx.doi.org/1.4168/aard.215.3.5.358 361
Kim JH, et al. Allergenicity of dandelion pollen kda 175 125 8 M 1 2 11 kda 7 kda 중하나인민들레꽃가루의감작률변화에대한추가적인연구가필요하다. 본연구에서민들레꽃가루내 IgE와결합하는 5개의알레르겐성분 (12 kda, 14 kda, 17 kda, 24 kda, 39 kda) 을확인하였다. 지금까지한명의환자에서 13 kda에서특이 IgE 결합성분을확인한국내보고가있다. 17) 본연구에서는혈청특이 IgE 항체가높은 22명 52 39 26 19 13 9 38 kda 24 kda 17 kda 14 kda 13 kda 12 kda Molecular weight of dandelion pollen (kda) 24 59.1* 14 22.7 12 17 22.7 18.2 13 9.1 38 4.5 5 1 15 No. of patients (%) Fig. 3. Sodium dodecyl sulphate-polyacrylamide gel electrophoresis findings of dandelion pollen extracts using 4% 2% gel. M, marker; 1, 4 μg of dandelion pollen; 2, 6 μg of dandelion pollen. Fig. 5. Frequency of IgE-binding components to dandelion pollen extracts by immunoblot analysis. *Indicates the IgE-binding component found in more than 5% of the allergic rhinitis patients tested. 1 2 3 4 5 6 7 8 9 1 11 12 13 14 15 16 17 18 19 2 21 22 N B kda 175 125 8 52 39 26 19 13 9 A B C D E Fig. 4. IgE immunoblot analysis of dandelion pollen extracts using sera of 22 patients with allergic rhinitis. M, marker; N, normal control; B, blank. A, B, C, D, and E according to Fig. 2. 362 http://dx.doi.org/1.4168/aard.215.3.5.358
김지혜외 민들레화분항원의교차반응과주요알레르겐 의환자를대상으로 IgE immunoblot 을시행한결과 5% 이상환 자에서관찰된하나의주요알레르겐 (24 kda) 을동정하였다. 꽃가루병환자의진료에서민들레꽃가루항원과다른꽃가루 항원간의교차항원성을확인하는것은원인항원확인과면역치 료에중요하다. 21) 국내에서가을철알레르기증상을유발하는대표 적인꽃가루항원인돼지풀과쑥꽃가루, 그리고환삼덩굴꽃가루 에대한다양한연구들이있으나대부분교차반응을나타내기보 다는, 각각의항원성에의한고유의반응으로간주한다. 3,22) 또한현 재까지의보고에따르면국내에서가을철꽃가루병의중요한원인 항원중의하나인환삼덩굴꽃가루도쑥과돼지풀꽃가루와교차 반응이없다. 1,23) 하지만 Weber 는국화과에속하는항원인쑥꽃가 루항원과국화및민들레꽃가루항원간에광범위한교차반응이 있으며이는 profilin 성분에의한것으로보고하였다. 21) 이러한잡 초꽃가루항원간의교차항원성은 profilin (14 kda), polcalcin (9 KDa) 및 lipid-transfer protein (1 kda) 와같은 panallergen 에의 해나타난다. 24) 국내의한연구에서도쑥, 국화 (Dendranthema grandiflorum) 그리고민들레꽃가루항원이쑥꽃가루항원에억 제되는것을확인하였다. 17) 한편본연구결과, ELISA 억제시험결 과 5 개의양상을관찰하였고, 이중일부환자군에서쑥과돼지풀 항원에의해유의한억제반응이관찰되었고, 이는항원간의교차 반응의가능성을시사한다. 또한 IgE immunoblot 상관찰된주요 알레르겐성분이 24 kda 이며이는쑥꽃가루항원의주요알레르 겐인 Art v1 (24 28 kda), 돼지풀꽃가루항원의주요알레르겐 (Amb a 1,27 kda) 과유사한분자량이유사하기때문에, 민들레꽃 가루와이두꽃가루간의교차반응을나타낼가능성이있다. 3,24) 명아주꽃가루항원의주알레르겐으로알려진 Che a 1 은 17 kda 이고환삼덩굴꽃가루항원의주알레르겐은 1 kda 및 18 kda 로 알려져있으며 25,26), 본연구에서관찰된민들레꽃가루항원의알레 르겐성분과유사하여일부환자에서관찰된명아주및환삼덩굴 꽃가루와의교차반응가능성을고려할수있고이에대한추가연 구가필요하다. 결론적으로본연구결과민들레꽃가루는가을철꽃가루병의 원인알레르겐일가능성을시사하며일부환자에서는단독감작에 의한원인항원으로고려해야한다. 또한쑥과돼지풀과같은잡초 꽃가루와의교차반응가능성이있어, 가을철에발생하는꽃가루 병환자의진료시이를고려해야한다. 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