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 Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 28  |  Issue : 1  |  Page : 40-46

Identification of different pigeon allergens and its trigger toward increase in inner city Asthma


Department of Immunology, Sir. H.N. Medical Research Society, Sir. H.N. Hospital and Research Centre, Girgaum, Mumbai, Maharashtra, India

Date of Web Publication11-Jun-2014

Correspondence Address:
Sudha Shrikant Deo
Senior Scientist, Sir. H.N. Medical Research Society, Sir. H.N. Hospital and Research Centre, Raja Ram Mohan Roy Road, Prathna Samaj, Girgaum, Mumbai - 400 004, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-6691.134224

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  Abstract 

Background: Upon exposure, allergic reactions to breathing pigeon feces are common. The dust of dried droppings irritates the nasal passages, causing sneezing, coughs, excess mucus and shortness of breath, dizziness and a sense of vertigo. Hence exposure to pigeon allergens in the surroundings has led to increase in hypersensitivity reactions due to pigeon proteins present in their feathers and droppings. Aims and Objectives: The aim and objective of the following study is to investigate the role of pigeon droppings in the increase of inner city asthma. To study the different allergens present in the pigeon droppings. Materials and Methods: A total of 500 asthmatics were screened for hypersensitivity reactions toward protein extracts from pigeon droppings. 100 asthmatic patients were selected showing 3+ reactions by skin scratch test and an induration of more than 5 mm with inflammation. Total immunoglobulin E (IgE) as well as specific IgE quantitated by enzyme-linked immunosorbent assay (ELISA) and circulating immunoglobulin G (IgG) antibody toward pigeon allergens was studied by western blot. Results: Totally 87 asthmatic patients and 23 healthy normal showed reactivity toward allergens of pigeon feathers and droppings by skin test with induration of 1.48 ± 0.12** in patients (P < 0.000) and 0.17 ± 0.81 in healthy controls. Reactivity shown toward pigeon dropping allergen was 13 ± 0.121 in patients and that shown by healthy controls being 0.26 ± 0.094*(P < 0.001), which was also statistically significant. The total IgE was 1906.84 ± 3696.27 IU/ml in patients **(P < 0.0001) when compared to healthy controls 86.21 ± 50.18 IU/ml. Specific IgE detected in patients toward allergens was 0.31 ± 0.10 OD. *(P < 0.001) to that of normal being 0.19 ± 0.06 OD. Patients serum reacted to 129 kD and 43 kD protein extract of pigeon dropping by western blotting and total IgG by ELISA was 1802.0 ± 66.5 mg/dl in patients (P < 0.016). The normal range being 581-1630 mg/dl. The pulmonary function test by spirometry was 60%, 40% lesser when compared with healthy normals. Conclusions: Observed results showed an increase in the hypersensitivity reactions toward the pigeon allergens and increase in the antibody levels of IgG in circulation. This probably may have added to the increase in asthma cases in our city.

Keywords: Allergens, immunoglobulin E, immunoglobulin G, pigeon allergens, proteins, skin test, western blot and enzyme-linked immunosorbent assay


How to cite this article:
Deo SS, Niphadkar PV, Ramesh S, Arora N, Kakade AM, Mulay C, Nadkar UL, Repal M, Prabhudesai S, Pandya V. Identification of different pigeon allergens and its trigger toward increase in inner city Asthma. Indian J Allergy Asthma Immunol 2014;28:40-6

How to cite this URL:
Deo SS, Niphadkar PV, Ramesh S, Arora N, Kakade AM, Mulay C, Nadkar UL, Repal M, Prabhudesai S, Pandya V. Identification of different pigeon allergens and its trigger toward increase in inner city Asthma. Indian J Allergy Asthma Immunol [serial online] 2014 [cited 2017 Mar 22];28:40-6. Available from: http://www.ijaai.in/text.asp?2014/28/1/40/134224


  Introduction Top


Exposure to dust from the pigeon loft can cause heterogeneity of diseases such as asthma, ornithosis, (microbial infections of birds which can be transferred to human beings), lung inflammation from inhaling irritant dusts. Allergic proteins are found in bird droppings and feather blooms. Few studies have shown that pigeon droppings are important source of antigen particularly in environmental. [1] Secreted IgA antibody are major protein antigen and intestinal protein mucin is the major carbohydrate antigen, The presence of immunoglobulin G (IgG) antibodies in symptomatic people and hypersensitivity reaction suggest complex immune mechanisms.

It is shown that keeping pigeons is an ancient and respected history for religious purpose, but there is a lack of awareness of associated infections and hypersensitivity disorders. Exposure to these birds can cause heterogeneity of diseases such as, (1) pigeon breeders syndrome, (2) alveolitis. [2]

It has been observed that occupational and environment exposure to pigeon has been quantitated using the UniCAP system for mix bird antigens and has been useful for diagnosis of allergic alveolitis. Studies have employed quantitative immunoelectrophoetic techniques, on sera from confirmed cases of pigeon breeders disease, to investigate the antigenicity of a pigeon bloom extract, implicated as a sensitizing agent in this disease. The major component has been identified as pigeon IgA and is partially cross-reactive to pigeon IgG. The presence of IgG antibodies in symptomatic people and exposure and onset of symptoms suggest complex pathogenic immune mechanisms involved, but no such studies have been conducted to detect immunoglobulin E (IgE) mediated immune response. [3],[4],[5] Hence, this study was undertaken to identify asthmatic patients showing hypersensitivity reactions to pigeon allergens and monitor the circulating antibody levels to understand the frequency of exposure and the cause of it that could be a useful guide to control or avoid the exposure to pigeons.


  Materials and methods Top


A total of 500 patients of asthma were screened for their hypersensitivity reaction to protein extracts of pigeon droppings and feathers and checked for their reactivity by skin scratch test. These included the residential people that included normal as well as asthmatic in and around the areas where pigeons harbored in the crevices of their buildings. The standard protein precipitation reactions were carried out and a known concentration, i.e., 1:10 dilution of this crude extract was used for sensitization of asthmatic patients and controls. From this 100 asthmatic patients who showed 3+ reaction by skin scratch test and measured by indurations and inflammation of more than 5 mm diameter were selected for our study. [6]

Inclusion criteria

Asthmatic patients with pigeon allergen positivity and abnormal clinical test results with bird exposure on daily basis were included.

Exclusion criteria

Patients with cardiovascular disease, tuberculosis, interstitial lung disease, asthmatic but pigeon allergy negative and showing history of smoking were excluded.

A total of 100 asthmatic patients (adults) were selected who were daily exposed to more than 3 pigeon every day. Totally 100 healthy individuals staying on the outskirts of the city were chosen as controls for comparison but not exposed to pigeons.

Study protocol

Group I

087 asthmatic patients were taken for the study as they were willing to get enrolled for the pulmonary function test (PFT) and were exposed to more than 3 pigeons every day.

Group II

Out of a total of 25 healthy normal, Only 23 healthy normals who showed exposure of more than 3 pigeons came for their PFT tests who volunteered for this project.

Patients

Clinical studies - PFT using Spirometer test.

Allergy studies

Reactivity to a panel of antigens obtained from pigeon droppings, pigeon feathers, fungus, dust mites and endotoxins were studied.

Immunological studies

IgG total, IgE total, IgE specific, white blood cell count and differential count.

Serum was obtained from the peripheral vein of 87 asthmatic patients which included 23 males and 64 females with age ranging from 20 to 70 years. 23 normals were included for comparison of data that included 7 males and 16 females. These were in the age range of 21-45 years as represents in [Table 1].
Table 1: Characteristics of asthmatic patients and healthy individuals

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Protein extraction

Protein extraction was done from the pigeon droppings as well as pigeon feathers. The crude extract was first defatted with diethyl ether, then extracted in 50 mM ammonium bicarbonate buffer pH 7.9, overnight at 4°C (1:20: Material:Buffer). The solution was centrifuged and the supernatant dialyzed overnight at 4°C against deionized water using a 3500 molecular weight membrane until a clear extract was obtained. This was then aliquoted in 1 ml and then lyophilized to a powder form for long storage. The protein was estimated and found to be 0.7 ug/ul [7],[8] and then reconstituted before use.

Skin scratch test was used as a test of hypersensitivity reactions. All patients were tested for a panel of 70 allergens and found to show 3+ reaction. IgE., a positivity toward antigens and then read for flare or indurations of >3 mm, which was considered positive.

For skin scratch test, 1 ml vial of antigen is diluted to 5 ml using sterile phosphate buffered saline and filtered through 0.22 um membrane to be used for scratch test. Each 1 ml vial may be diluted to 0.5 ml in 50% glycerol buffer solution and when required removed to be used for scratch test (Company-Creative drug industries Navi Mumbai-400705). [9] The 100 healthy individuals staying on the outskirts of the city that were chosen as controls for comparison but not exposed to pigeons did not show any reactivity and thus did not include in our study.

Total IgE

Serum IgE levels were estimated in all the subjects taken for the study by enzyme-linked immunosorbent assay (ELISA) using kits from RADIM diagnostics (Italy). The standard protocol was used for quantitation of IgE. [10]

Specific IgE

Specific IgE was also studied in the above mentioned study group. This was studied using the pigeon dropping allergen and ELISA kits from CARLA-SYSTEM of RADIM diagnostics - Italy. [11]

Total IgG

ELISA assay, the solid phase indirect ELISA used for the detection of IgG antibodies to pigeon dropping antigens was based on that described by Volker et al. method. [11],[12],[13]

SDS-PAGE assay sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) analysis and western blot for detection of the molecular weight of the protein band present in the pigeon antigens that causes sensitization. SDS-PAGE is performed by the following method. Briefly 7.5% of resolving gel is prepared containing (29% w/v acrylamide and 1% bisacrylamide in a 1.5 M Tris HCl buffer pH 8.8, 10% SDS and 10% ammonium persulfate with 10 ul of tetramethylethylenediamine added just before making the volume with milli-Q water). The gel is poured through the glass plates up to the desired level. The resolving gel was covered with water saturated with butanol to keep the gel surface straight so that there is a flat and sharp interface.

Assay of western blot.T Assay of western blotting this was performed according to the method of Towbin et al. [14]

Immunoassay by electrochemical detection was done for all the samples and controls. [15]

Spirometry an important tool used for generating pneumotachographs. [16] Spirometry measures air movement, which is the most commonly prescribed PFT.

Forced expiratory volume

FEV 1 is the amount of air that can be forcefully exhaled in the first second, describes the severity of lung disease.

Forced vital capacity

FVC is the total amount of air that can be forcefully blown out after taking a deep breath as possible, which indicates how much air the lungs can hold.

FEV 1 /FVC is the ratio of the amount of air forcefully exhaled in the first second divided by the total amount of air forcefully exhaled. Using the patient's spirometer readings is the lung's normal air capacity or obstructive. Capacity was determined. FEV 1 80-100%: Normal FEV1 60-79%: Mild FEV 1 40-59%: Moderate FEV 1 35-40%: Severe FEV 1 <35%: Very severe.

Nasal provocation test (NPT) is the assessment of allergic symptoms and detection of air capacity. The nasal challenge test (i.e., NPT) for confirming/excluding allergic rhinitis and causative allergens involves applying a small amount of allergen solution directly to the nares. If the initial nasal allergen response is negative then after 15 min, the extract concentration is increased 3-fold. Doses are increased every 15 min in this fashion until a positive result is obtained, or until maximum concentrations have been administered with no response. Response to the allergen is determined by nasal peak expiratory flow rate, number of sneezes and presence of rhinorrhea. [17]

In this the concentrated dose of the pigeon allergen is applied to the nostrils and passive expiratory volume is then noted to observe the nasal obstruction in these patients.

Statistical analysis

SPSS package of version 16 was used for analyses of the data and statistical significance was calculated.

The project was approved by the Institutional Scientific Advisory Committee and informed consent was taken from the patients.


  Results Top


[Table 1] shows the characteristics of the asthmatic patients and the healthy individuals taken for our study. We studied our pigeon allergen by skin scratch test on 87 diagnosed patients of asthma. And 23 age matched healthy individuals. Of the 87 asthma patients, 23 were males and 64 females with age ranging from 20 to 70 years. The 23 healthy individuals in the same age range of 21-45 years consisted of 7 males and 16 females. The reactivity of these patients and the healthy normal was studied toward the 2 Pigeon allergens namely (a) pigeon feather allergen and (b) pigeon dropping allergen.

[Table 2] represents the reactivity of the patients and healthy individuals toward the 2 pigeon allergens by skin scratch test, the release of total IgE in the serum and its reactivity toward specific IgE as detected by ELISA. We observed very significant reactivity by patients toward feather allergens 1.48 ± 0.12/0.17 ± 0.81 (P < 0.0001) as well as pigeon droppings 1.13 ± 0.12/0.26 ± 0.09 (P < 0.001). The total IgE being 1906.84 ± 3696.27/86.21 ± 50.18 (P < 0.0001) as well as the specific IgE. 0.31 ± 0.10/0.19 ± 0.06 (P < 0.0001) is also highly very significant.
Table 2: Reactivity to pigeon allergens by skin test, the total IgE (IU/ml), specific IgE (OD), in asthmatic patients and controls

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[Table 3] gives the reactivity's shown by the 28 patients who were selected on the basis of high IgE and specific IgE. The reactivity's of these positive serums toward extract of antigen from pigeon droppings was studied using western blot analysis. Among the 28 patients, 22 patients showed strong reactivity toward 43 kD protein band in the antigen. Similarly 23 healthy normals taken for study only 3 reacted toward the same 43 kD band. 17 patients and 1 healthy normal showed strong reactivity toward 129 kD protein band. We have not identified the type of protein present in the 43 kD and 129 kD protein bands. Future studies will involve the identification of these specific bands.
Table 3: Reactivity of the serum from asthmatic and normal individuals toward the different antigens from pigeon droppings studied by western blot

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[Table 4] gives the comparative data of patients PFT with respect to total IgE range. The total IgE is then divided into three groups as 300-1000 IU/ml, 1001-5000 IU/ml and 5001-10000 IU/ml. We observed that though the maximum number of patients showed IgE in the first group the percentage positivity of this group was 28.74% which was more or less similar to 27.58% of the second group. There was no difference in the specific IgE in all the three groups while the 3 rd group had low, i.e., 68.55% of pulmonary function activity. Normal pulmonary function shown by healthy individuals is usually 100%; hence patients of asthma have shown 40% low activity i.e. 60% only.
Table 4: Total IgE specific IgE and PFT according to different concentrations of total IgE

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As it can be seen from [Table 5], the quantitation of total IgG in the circulatory serum on exposure to these antigens was studied by indirect ELISA and was established using the standard ELISA kit for IgG. This was conducted to observe the immune response after exposure to antigens. The total IgG shown by all the IgE positive patients being 1802.0 ± 66.5 which is highly significant when compared with healthy normal with a mean of 605 mg/dl.
Table 5: Total IgG as studied by indirect ELISA assay in asthmatic patients and healthy controls

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[Table 6] summarizes the positive cases of asthmatic patients toward the reactivates to pigeon allergens by the different tests undertaken for our research. We observed 53% of positive cases toward spirometry. 81% of cases showed low to good pulmonary function, 51% reacted toward pigeon droppings and 67% toward pigeon feathers respectively. Nearly 64% had high IgE and only 18% had high specific IgG, while 64% of these patients had higher circulating IgG.
Table 6: Percentage positive cases of asthmatic patients showing allergic reactions toward pigeon antigens

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On the whole we observed that these individuals had definitely higher reactivity toward these allergens compared with the reactivity shown by healthy individuals. Hence we may add that there is a possibility that these patients may have been exposed to these allergens which could have been a trigger leading to the increase in the inner city asthma.

[Figure 1] and [Figure 2] have shown positive reactivity toward pigeon droppings by western blot.
Figure 1: Blot picture showing the reactivity of asthmatic patients toward the pigeon allergen. The center lane shows the prestained markers

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Figure 2: Reactivity shown by 5 asthmatic patients and 3 healthy normals toward pigeon allergens by western blot

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  Discussion Top


This study confirms the presence of pigeon related antibodies shown by asthmatic patients. We also observed specific IgE reactivity confirming that these asthmatic patients are definitely exposed to pigeon antigens which may have added to the increased trigger of asthma in our Mumbaites. None of the seras from the healthy normal individuals demonstrated any reactivity toward any of the proteins present in the pigeon allergens as shown in [Figure 2]. The PFT also revealed that these patients had low lung functional activity as compared to healthy individuals.

Studies published have shown that exposure to common indoor allergens such as dust mites, cats, dogs and fungi can worsen asthma and allergies. [17] Recent studies have demonstrated that high exposures to cockroaches and mouse allergens often occur in inner-city dwellings and that exposure to cockroaches and mouse allergens are associated with higher rates of asthma. Thus pigeon allergens may also play an important role in worsening asthma in certain urban environments where pigeons harbor. This study is similar to the study conducted by Curtis et al. [18] which measured or identifies that there are certain pigeon allergens in the pigeon droppings which are harmful or can increase the risk of asthma. [2]

This study is the first study in India and we have tried to identify different protein bands that are found in the pigeon antigens. Studies conducted by Mcsharray et al. 2000 [19] suggests that there are multiple antigens that have been extracted from the pigeon droppings. Feathers, serum, egg yolk and white, crop fluid and gut wall. By cross-absorption, the major antigens were demonstrated in the gamma globulin fraction of pigeon serum and these had immunological identity with IgA in droppings and on the dust extruded from feathers called bloom. This consists of inert keratin particles 1 μ in diameter which carry serum proteins. The presence of IgG antibodies in our patients is similar to published literature that state that in symptomatic people presence of IgG is seen and a delay between exposure and onset of symptoms suggest complex pathogenic immune mechanisms. The level of serum IgG antibodies against pigeon antigens reflects the level of antigen exposure. [20],[21],[22],[23],[24]


  Conclusion Top


The presence of feral pigeons in urban habitat and their degree of interactions with human life and activities can be perceived in many ways, ranging from harmless and tame birds to harmful pests, depending on the personal cultural background (Jerolmack 2008; Johnston and Janiga, 1995). Nevertheless, feral pigeons have a formidable capacity to become pest by any standard method. Factors that have been identified as important in becoming a pest include the main characteristics of pigeons, such as being a granivore, having an alimentary storage crop, high reproductive rate, colonial habits and group foraging. [25],[26]

Feral pigeons are of considerable epidemiological importance, being reservoirs and potential vectors of a large number of microorganisms and source of antigens of zoonotic concern, causing both infections and allergic diseases that can be lethal.

Pathogens can be transmitted to humans mainly via excreta, secretions, or dust from feathers spread into the environment. Thus a direct contact with pigeons can be unimportant. Pigeons breeding and roosting sites host an endless number of arthropods that may infest humans as bugs fleas, mites and ticks. The latter are of particular human concern, as the soft tick Argas reflexus.

It is seen that pigeon droppings cause mess on the surfaces and their content can eat into soft stone and cause long term damage to buildings. The nest droppings and feathers also block rainwater pipes causing damage by water clogging. Pigeon allergens may also play an important role in worsening asthma in certain urban environments which contain many pigeons.

Besides these droppings spoil the pavements as make it slippery and becomes difficult for elders to walk and thus droppings carry pathogenic organisms. In all feeding pigeons is considered as an unhygienic and anti-social practice. Feeding pigeons encourages them to gather in increasing number that adds to nuisance and annoyance. This also causes the pigeons to be dependent on human beings. Feeding pigeon often ends up feeding more pigeons and hence the increase in the food grains needed for them, as a result at times there is excess left over causing the remaining food to go bad and it may attract more rats and mice thus causing the spread of disease to humans. Further the government should take the necessary steps in controlling the influx of pigeons.

The ideal method to control asthma would be to control feeding these pigeons and hence limiting the supply of food grains to birds by natural means and thus reduce the breeding rate and discourage the influx of pigeon from different areas.

 
  References Top

1.Baldwin CI, Stevens B, Connors S, Todd A, Bourke SJ, Calvert JE, et al. Pigeon fanciers′ lung: The mucin antigen is present in pigeon droppings and pigeon bloom. Int Arch Allergy Immunol 1998;117:187-93.  Back to cited text no. 1
    
2.Curtis L, Lee BS, Cai D, Morozova I, Fan JL, Scheff P, et al. Pigeon allergens in indoor environments: A preliminary study. Allergy 2002;57:627-31.  Back to cited text no. 2
    
3.Lopata AL, Schinket M. Allergy in workplace. Curr Allergy Clin Immunol 2004;17:87-90.  Back to cited text no. 3
    
4.Bheekha Escura R, Wasserbauer E, Hammerschmid F, Pearce A, Kidd P, Mudde GC. Regulation and targeting of T-cell immune responses by IgE and IgG antibodies. Immunology 1995;86:343-50.  Back to cited text no. 4
    
5.Longbottom JL. Pigeon breeders′ disease: Quantitative immunoelectrophoretic studies of pigeon bloom antigen. Clin Exp Allergy 1989;19:619-24.  Back to cited text no. 5
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6.Huizinga M, Lubbers M, Berrens L. Detection of precipitating and complement consuming antibodies by enzyme linked immune sorbent assay in pigeon breeders′ disease. Immunobiology 1984;166:168-76.  Back to cited text no. 6
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7.McCormick DJ, Fredricks WW, Tebo TH, Calvanico NJ. The antigens of pigeon breeder′s disease. VII. Isoelectric focusing studies on unfractionated pigeon dropping extract. J Immunol 1982;129:1493-8.  Back to cited text no. 7
    
8.Fredricks WW, Tebo TH. The antigens of pigeon breeder′s disease. I. Studies on unfractionated pigeon dropping extracts. Int Arch Allergy Appl Immunol 1977;53:214-21.  Back to cited text no. 8
    
9.Fredricks WW, Tebo TH. The antigens of pigeon breeder′s disease. III. Immunologically related antigens of pigeon dropping extracts: PDE1, 2, A and B. Int Arch Allergy Appl Immunol 1980;61:65-74.  Back to cited text no. 9
    
10.Deo SS, Mistry KJ, Kakade AM, Niphadkar PV. Relationship of total IgE, specific IgE, skin test reactivity and Eosinophil′s in Indian patients with allergy. J Indian Acad Clin Med 2010;11:265-71.  Back to cited text no. 10
    
11.Volker A, Bidwell D, Bartlett A. Microplate immunoassay for the immunodiagnosis of virus infections. In: Rose NR, Friedman HH, editors. Handbook of Clinical Immunology. Washington, D.C.: American Society for Microbiology; 1976. p. 506-12.  Back to cited text no. 11
    
12.Tebo TH, Moore VL, Fink JN. Antigens in pigeon breeder′s disease: The use of pigeon dropping antigens in detecting antibody activity. Clin Allergy 1977;7:103-8.  Back to cited text no. 12
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13.Grabski AC, and Burgess RR. Preparation of Protein Samples for SDS-Polyacrylamide Gel Electrophoresis: Procedures and Tips. InNovations, 2001;13:10-2.  Back to cited text no. 13
    
14.Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci U S A 1979;76:4350-4.  Back to cited text no. 14
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15.Dickinson J, Fowler SJ. Quantification of proteins on western blots using ECL. Available from: "/book/10.1385/1592591698" The Protein Protocols Handbook 2002, p. 429-37.  Back to cited text no. 15
    
16.Galant SP, Morphew T, Newcomb RL, Hioe K, Guijon O, Liao O. The relationship of the bronchodilator response phenotype to poor asthma control in children with normal spirometry. J Pediatr 2011;158:953-9591.  Back to cited text no. 16
    
17.Alonso-Llamazares A, Martinez-Cócera C, Domínguez-Ortega J, Robledo-Echarren T, Cimarra-Alvarez M, Mesa del Castillo M. Nasal provocation test (NPT) with aspirin: A sensitive and safe method to diagnose aspirin-induced asthma (AIA). Allergy 2002;57:632-5.  Back to cited text no. 17
    
18.Curtis L, Lee BS, Cai D, Morozova I, Fan JL, Scheff P, et al. Pigeon allergens in indoor environments: A preliminary study. Allergy 2002;57:627-31.  Back to cited text no. 18
    
19.McSharry C, Anderson K, Boyd G. A review of antigen diversity causing lung disease among pigeon breeders. Clin Exp Allergy 2000;30:1221-9.  Back to cited text no. 19
    
20.Moore VL, Fink JN. Immunologic studies in hypersensitivity pneumonitis - Quantitative precipitins and complement-fixing antibodies in symptomatic and asymptomatic pigeon breeders. J Lab Clin Med 1975;85:540-5.  Back to cited text no. 20
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21.Fink JN, Moore VL, Barboriak JJ. Cell-mediated hypersensitivity in pigeon breeders. Int Arch Allergy Appl Immunol 1975;49:831-6.  Back to cited text no. 21
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22.Baldwin CI, Calvert JE, Todd A, Bourke S, Allen A. IgG subclass responses to pigeon intestinal mucin in pigeon Fanciers′ lung Eur J Med Res 2000;5:128.  Back to cited text no. 22
    
23.Baldwin CI, Todd A, Bourke SJ, Allen A, Calvert JE. Pigeon fanciers′ lung: Identification of disease-associated carbohydrate epitopes on pigeon intestinal mucin. Clin Exp Immunol 1999;117:230-6.  Back to cited text no. 23
    
24.Todd A, Coan R, Allen A. Pigeon breeders′ lung; IgG subclasses to pigeon intestinal mucin and IgA antigens. Clin Exp Immunol 1993;92:494-9.  Back to cited text no. 24
    
25.Jerolmack C. How pigeons became rats: The cultural-spatial logic of problem animals. Soc Probl 2008;55:72-94.  Back to cited text no. 25
    
26.Johnston RF and Janiga M. (1995). The Feral Pigeons, Oxford University Press, ISBN 0195084098, London.  Back to cited text no. 26
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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