Bites of the European pigeon tick (Argas reflexus): Risk of IgE-mediated sensitizations and anaphylactic reactions

Article Outline

• Abstract
• Methods
  • Study population
  • Questionnaire
  • Allergen source and preparation
  • SPT
  • Measurements of allergen specific IgE
  • Allergen characterization by electrophoresis, IgE immunoblot, and expression of recombinant Arg r 1
  • Statistical analysis
• Results
  • Local reactions are predominant after a bite of the soft tick Argas reflexus
  • Severe SRs are less common after an Argas bite
  • Infrequent SPT results with a whole-body extract of Argas
  • Specific IgE to allergens of Argas
  • Poor agreement between SPT and allergen specific IgE to Argas
  • Atopic predisposition as a risk factor for IgE-mediated sensitizations to Argas
  • IgE immunoblot experiments, IgE binding, and further allergen characterization
• Discussion
• Acknowledgment
• Appendix. Supplementary data
• References
• Copyright

Background

Local and systemic reactions can occur after bites of Argas reflexus (Argas), a soft tick parasitizing pigeons.

Objective

Risk assessment of IgE-mediated sensitizations and systemic reactions after Argas bites.

Methods

Case histories, skin prick tests (SPTs) with a whole-body extract of Argas containing major allergen Arg r 1, and common inhalants and specific IgE measurements were obtained from 148 subjects who had had Argas bites and 20 volunteers as a control group.

Results

Systemic reactions (urticaria, angioedema, dyspnea, cardiovascular dysregulation, unconsciousness) were reported in 12 of 148 (8%); 146 of 148 (99%) had local reactions. Atopy was found in 37 of 146 (25%) with local reactions and 3 of 12 (25%) with systemic reactions. SPT to Argas was positive in 24 of 148 (16%) with a high proportion of atopics 10 of 24 (42%); specific IgE to Argas was detectable in 12 of 135 (8% of 148) with moderate concordance to systemic reactions. No positive SPT or specific IgE results to Argas were obtained in the control group. Immunoblotting of 23 sera revealed an IgE-binding protein in 19 of 23 sera (82%) at 22 kd, indicating a major allergen of Argas.

Conclusion

Severe anaphylactic reactions were infrequently (approximately 8%) found after bites of the soft tick Argas reflexus. Atopy is a risk factor for skin sensitizations to Argas, but not for systemic reactions after bites by Argas. Using a whole-body extract of Argas, diagnosis through SPT and specific IgE is hampered by false-negative and irrelevant positive results, particularly in atopy.

Key words: Arthropod allergy, pigeon tick, Argas reflexus, tick bite, IgE-mediated reaction, anaphylaxis, whole-body extract, skin prick test, allergen specific IgE

Abbreviations used: LR, Local reaction, NPV, Negative predictive value, PPV, Positive predictive value, r, Recombinant, SPT, Skin prick test, SR, Systemic reaction

Bites of the European pigeon tick (Argas reflexus; Fig 1) can cause local inflammatory reactions, but also anaphylactic systemic reactions (SRs). Argas reflexus (Argas) is a soft tick, having a life span of as long as 10 years, while feeding on blood only once or twice per year.¹, ² Without eating, it can survive for 3 to 5, maximally 9 years. Its survival capabilities are based on specific features: (1) low metabolism, (2) extremely low whole-body water loss rates,³ (3) discontinuous ventilation,⁴ and (4) formation of stable aggregations within microsites like wall cracks and wooden clefts. Finally, it is (5) resistant to low temperatures as well as heat.⁵, ⁶

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• Fig 1. 

  European pigeon tick (Argas reflexus). Dorsal (left) and ventral view (right). Scale: millimeter.

Because of the growing number of feral domestic pigeons in Middle and Southern Europe, infestations of pigeon breeding sites by Argas became an increasing problem. From microhabitats in the vicinity of pigeon breeding sites in buildings, Argas will seek and accept human beings as a substitute host after removal of pigeons or in case of overpopulation of Argas.

Severe reactions after an Argas bite have repeatedly been reported⁷ in European countries: France,⁸, ⁹ Germany,¹⁰, ¹¹ Italy,¹² Poland, and Switzerland.¹³ Bites usually occur at night because of the nocturnal activity of the tick. Severe allergic reactions with cutaneous, respiratory, gastrointestinal, and cardiovascular symptoms requiring immediate emergency treatment and subsequent hospitalization have been described in 12 cases in France.¹⁴ Allergen specific IgE to Argas allergens was demonstrated by using a whole-body extract.¹⁵ It had been speculated that children, elderly people, or atopic individuals have an increased risk to develop an IgE-mediated immune response to Argas allergens. However, no data exist about such a risk. A high number of infested buildings together with frequent reports of tick bites in citizens of Leipzig, Germany, prompted us to evaluate the risk of allergic sensitizations and anaphylactic SR after an Argas bite. In addition, the utility of skin prick test (SPT) and specific IgE measurements were investigated.

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Methods 

Study population 

Print, radio, and television media promoted the recruitment of volunteers interested in participating in the study, which was approved by the ethics committee of the university. After informed and written consent, individuals were included in the study depending on their clinical case history suggestive for pigeon tick bite reactions:

In total, 148 individuals, 90 female and 58 male subjects, were examined over a period of 2 years. Their age ranged from 7 to 80 years (average, 36 years). Twenty volunteers without any bite reaction served as a control group.

Questionnaire 

Specific questions were addressed by using a standardized questionnaire. Basic data like age, sex, and location of the apartment where the bite reactions took place were recorded. Special emphasis was put on information about former or current pigeon breeding sites close to the living space and pigeon tick infestations. The family history with regard to immediate-type allergies and the individual atopic predisposition was requested. Extensive case reports of each bite reaction were established through questions for each local and/or SR, subsequent symptoms, time, course and individual medical and emergency treatment, if necessary.

Allergen source and preparation 

Several hundred specimens of adult pigeon ticks were collected and frozen at −20°C. After homogenization, the whole-body extract was prepared. After extraction (1:10 in 125 mmol/L NH4HCO₃, overnight at +5°C), the extract was centrifuged, filtrated, and dialyzed 3×/day against 5 mmol/L NH₄HCO₃ and 1 day against milliQ H₂O before lyophilizing. A final protein detection revealed 300 mg lyophilized allergenic material stored at −70°C.

SPT 

For SPT, 2 mg was reconstituted in 0.5 mL sterile Coca solution (0.5% wt/vol NaCl, 0.25% wt/vol NaHCO₃) without phenol. The solution was filtrated through a sterile 0.22-μm filter, and an equal volume (0.5 mL) of sterile glycerol was added. SPTs were performed on the volar forearm by using common inhalant allergens (ALK-Abelló, Hørsholm, Denmark) to determine the atopic risk: birch, grass, and mugwort pollen; dust mites Dermatophagoides pteronyssinus and farinae; cat dander; and Alternaria alternata. Histamine-hydrochloride (10 mg/mL) and normal saline, both supplemented with 50% vol/vol glycerol, served as controls. Reactions were evaluated after 20 minutes, documenting wheal sizes with a marker pen and a strip of tape. Average wheal diameters were calculated by the mean of the largest and smallest diameter. An average of 3 mm or larger was considered a positive result. One or more positive skin reactions to common inhalants indicated an increased risk of atopic predisposition.

Measurements of allergen specific IgE 

Using pigeon tick specimen from Italy, allergens from Argas had been previously extracted and coupled to a solid phase (ImmunoCAP) according to an internal protocol (Pharmacia Diagnostics, Uppsala, Sweden). Serum measurement of allergen specific IgE was performed according to the manufacturer's instructions. Cutoff value was considered 0.35 kU/L of IgE. Levels above this threshold indicated circulating IgE to Argas allergens.

Allergen characterization by electrophoresis, IgE immunoblot, and expression of recombinant Arg r 1 

Ten milligrams of lyophilized Argas extract (ALK-Abelló) were dissolved in 1 mL PBS and incubated for 3 minutes in an ultrasonic bath. Insoluble particles were excluded by centrifugation 30,000g, 30 minutes, 4°C, before protein concentration was determined.¹⁶ One-dimensional SDS-PAGE and IgE-specific immunoblot analysis of pigeon tick extract were performed by using 300 μg protein on a 10% NuPAGE Bis-Tris gel (Novex, San Diego, Calif) under reducing conditions as described recently.¹⁷ In addition, 2-dimensional electrophoresis of the Argas extract with IgE blotting, expression of recombinant (r) Arg r 1, a recently described major allergen,¹⁸ as a fusion protein, subsequent IgE binding, and inhibition studies have been performed and described (see Methods and Results in the Online Repository at www.jacionline.org).

Statistical analysis 

Qualitative results were depicted by 2 × 2 tables; statistical significance was calculated by χ² test. The statistical significance of different values between different groups was analyzed by using the Mann-Whitney U test. Association between 2 parameters was determined by Spearman rank test. Values were considered significant at P < .05.

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Results 

Local reactions are predominant after a bite of the soft tick Argas reflexus 

During a period of approximately 2 years, 148 subjects with suspected bites by the soft tick Argas were included in a retrospective study to estimate the frequency of severe allergic reactions and determine the rate of IgE-mediated sensitizations to allergens of Argas. Specific questions revealed individual bite reactions ranging from 1 to approximately 30, with an average of 5 ± 0.5 (mean ± SEM) per person, related to neither sex (P_s = .9) nor individual age (P_s = .7). Former or current pigeon breeding sites close to their apartment (eg, in the attic) were reported by 130 individuals; 99 knew of past or current pigeon tick infestations, and 133 people had found Argas in their apartment, 128 more than once. Nearly all subjects (146/148) had had local reactions (LRs; Table I), varying from small papular nodes with local itching to grotesque, painful swellings or superinfected lesions eventually becoming purulent abscesses or resulting in massive local lymphatic inflammation.

Table I. LRs and SRs after a bite of the pigeon tick Argas reflexus in 148 subjects (37 atopics, 24%, and 111 nonatopics)

	Frequency
Symptoms	n	%
Local	146	99
Redness	142	96
Local itching	124	84
Inflammatory node	93	63
Lymphatic secretion	36	24
Wheal	25	17
Pruritic secretion	20	14
Lymphangitis	12	8
Lymph node swelling	10	7
Vesicle	10	7
Systemic	12	8
Urticaria	11	7
Angioedema	6	4
Vascular dysregulation	2	1
Dyspnea	7	5
Unconsciousness	4	3
Gastrointestinal symptoms	3	2
Rush with pruritus	3	2

Severe SRs are less common after an Argas bite 

Systemic reactions turned out to be much less common than LRs. Determined by critical evaluation of the case histories, only 12 of 148 (8%) developed systemic symptoms, most likely associated with an Argas bite (Table I). Cutaneous reactions with urticarial hives and itching were reported frequently (11/12), sometimes associated with swelling of the face—that is, eyelids and lips, representing angioedema. In addition, dyspnea, gastrointestinal symptoms like nausea or diarrhea, and severe vascular dysregulation occurred in some of the individuals, occasionally leading to unconsciousness (4/12). SRs were associated with the total number of bite reactions (P < .001), but also with female sex (P < .001).

Infrequent SPT results with a whole-body extract of Argas 

None of the control subjects showed a positive SPT response to the extract containing allergens of Argas. Using the same extract, variable results were obtained in 24 of 148 (16%) subjects with a history of Argas bite reactions, ranging from a wheal of 12.5 mm to no detectable skin response (0-mm wheal) in the majority of the individuals tested (Fig 2). A positive SPT result was obtained in 8 of 12 with a SR; however, 3 subjects with SR did not show any and 1 individual only a weak SPT response (wheal < 3 mm) to Argas allergens. A substantial number of subjects without reported SR (16/136) reacted with either small (<3 mm) or significant (≥3 mm) SPT wheals as large as 8 mm (Fig 2). On the basis of a suggestive case history for SR, SPT to Argas was hampered by false-positive and false-negative results, providing a diagnostic sensitivity of 67% and a specificity of 88% (Table II, upper left portion). The positive predictive value (PPV; 33%), referred to the study population of patients with SR to Argas bite, turned out to be much lower than the negative predictive value (NPV; 97%), implying that skin test reactivity in subjects with an Argas bite reaction does not necessarily reflect an allergic reaction of clinical relevance, but that negative SPT responses do most likely exclude an anaphylactic SR, because of the rather low proportion of SR after an Argas bite.

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• Fig 2. 

  Skin test results obtained with a whole-body extract of the soft tick Argas reflexus. syst, Systemic reactions; loc, local reactions.

Table II. Relationship among SRs after Argas bites, diagnostic results, and status of atopy

	SPT			IgE
	+	−		+	−
SR			SR
+	8	4	+	5	7
−	16	120	−	7	116∗
Sensitivity 67% PPV 33%			Sensitivity 42% PPV 42%
Specificity 88% NPV 97%			Specificity 94% NPV 94%

	SPT			SR
	+	−		+	−
IgE			Atopy
+	10	2	+	3	34
−	14	109∗	−	9	102∗

Specific IgE to allergens of Argas 

Specific IgE levels to Argas were detected in 135 sera; 13 were missing. No detectable IgE was found in 20 control subjects. In contrast, some individuals with a suggestive history (12/135; 9%) demonstrated allergen specific IgE levels above 0.35 kU/L. Only 5 of 12 with detectable IgE, ranging from levels as low as 0.44 to values of 68 kU/L (Fig 3), had reported SR. On the other hand, 7 individuals reporting SR to Argas were not picked up by allergen specific IgE (Table II, upper right portion). Again, on the basis of a suggestive case history for SR, test sensitivity (42%) and specificity (94%) of allergen specific IgE values as well as PPV (42%) and NPV (94%) do not result in high diagnostic efficacy. However, because of the low estimated prevalence of SR to Argas, allergen specific IgE measurements are more effective in excluding an allergic SR.

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• Fig 3. 

  Allergen specific IgE to Argas reflexus. syst, Systemic reactions; loc, local reactions.

Poor agreement between SPT and allergen specific IgE to Argas 

Comparing positive results from either SPT or IgE measurements revealed no close association between immediate-type wheal responses and allergen specific IgE levels to Argas (Fig 4). General qualitative agreement (concordance, 88%) was hampered by a significant number of positive reactions (n = 14) with no detectable IgE (Table II, lower left portion). Ten subjects showed concordant positive results; 2 individuals with specific IgE failed to respond to the SPT with Argas.

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• Fig 4. 

  Association between individual SPT results (x-axis) and detection of IgE to Argas (y-axis). syst, Systemic reactions; loc, local reactions.

Atopic predisposition as a risk factor for IgE-mediated sensitizations to Argas 

Relating the risk of SR to Argas allergens to the atopic predisposition did not reveal any close association (Table II, lower right portion). The proportion of atopic subjects with SR to Argas allergens (3/12; 25%) did not differ from the ratio of atopic subjects within the whole group (37/148; 25%). However, a positive SPT to Argas allergens occurred in 10 atopic versus 14 nonatopic individuals, indicating a trend to more frequent skin reactions to Argas allergens in atopics.

IgE immunoblot experiments, IgE binding, and further allergen characterization 

Applying different SDS-PAGE conditions the SPT extract revealed a dominant protein component at about 22 kd plus thin protein bands at 50, 68, and 90 kd and additional bands at 10 and 12.5 kd under denaturing conditions (see Results and Fig E1 in the Online Repository at www.jacionline.org).

The dominant role of the 22-kd Argas allergen was supported by a high frequency of IgE binding in Argas-sensitized subjects. A 22-kd protein was recognized by 19 of 23 sera (Fig 5). Sera of patients without binding of the 22-kd protein recognized either a single allergen at 40 kd (Fig 5, lane 16) or a single allergen at 44 kd (Fig 5, lane 15) or no protein component (Fig 5, lane 21+22). No association occurred between individual IgE binding profiles and clinical symptoms or sensitivity of the patients.

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• Fig 5. 

  IgE blot of Argas proteins incubated with sera of subjects sensitized to Argas (lane 1-23), buffer control (lane 24).

The IgE-binding protein at 22 kd revealed several isoforms after 2-dimensional electrophoresis and blotting (see Results and Figs E3 and E4 in the Online Repository at www.jacionline.org). In addition, selected sera recognized a rArg r fusion protein (see Fig E5 in the Online Repository at www.jacionline.org) expressed from mRNA/cDNA of salivary glands in Western blot experiments (see Results and Figs E6 and E7 in the Online Repository at www.jacionline.org) and in an IgE solid phase binding assay. Preincubation with the Argas extract inhibited the IgE binding to the rArg r 1 fusion protein, indicating that Arg r 1 is a component of the extract used for SPT (see Methods and Results in the Online Repository at www.jacionline.org).

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Discussion 

Because of an extraordinarily high number of pigeon and Argas-infested buildings with damaged attics, the city of Leipzig presumably had the highest rate of bite reactions in human beings compared with other places in Europe.¹⁹ Despite the fact that only 12 of 148 (8%) reported SR after Argas bites, this number could still be overestimated because of the design of the study. Because the subjects were not randomly collected but actively asked for their participation, a selection bias might have led to an overestimation of SR: severely affected individuals are more likely to respond to the invitation of such a study. This might lead to high proportions, like >50% SRs after a bite of the jack jumper ant reported by a retrospective questionnaire-based study from Tasmania, New Zealand.²⁰ False-positive case histories can potentially corrupt the numbers of prevalence and diagnostic efficacy of subsequent allergy tests. Various reasons might lead to false-positive case histories: (1) unintentional overestimation of large LRs, (2) reactions modulated by serve anxiousness of the subject, and (3) purposeful false-positive histories for secondary disease benefits.

Interestingly, related models after an insect sting provide similar ratios of SRs comparable with our data. In the general population, 1.5% to 3% report SRs to Hymenoptera venom.²¹, ²² The epidemiology of allergic reactions to the imported fire ant in endemic areas²³ is far from clear²⁴ and illustrates the difficulties in estimating the number of clinically relevant allergic reactions after arthropod stings or bites. Despite careful interviews, an uncertain degree of overestimation of SR cannot be ruled out, because severe reactions after a presumed bite of Argas could not be confirmed by challenge procedures.

Using a whole-body extract from Argas for SPT could create inherent problems of nonstandardized material. No one in the control group showed a reaction to Argas, because small molecules were removed by dialysis to exclude irritating components, but low-molecular-weight allergens could have been lost too. In addition, the allergenic proteins might represent only a minor proportion of the extract, leading to false-negative results in individuals with low-grade sensitivity. The high proportion of positive skin responses—even in subjects without SRs after an Argas bite—is indicative of the biological activity of the extract, an observation similar to whole-body extracts of the imported fire ant used for skin test purposes²⁴; however, false-negative reactions cannot be ruled out, because no former experience with the extract existed. In analogy to Hymenoptera hypersensitivity, where venom extracts dramatically increased the diagnostic efficacy of skin test reagents compared with whole-body extracts,²⁵ an Argas extract from the salivary glands (as much as 1/10 of the whole body weight) of the soft tick might also improve SPT results.

A whole-body extract of Argas species from Italy has also been used for the development of solid phase–coupled allergens for further in vitro testing. These tests provided quantitative IgE levels to Argas allergens, not showing elevated levels in the control group. However, because the quality of such a test largely depends on the allergenic material used, analytical sensitivity can be limited in the case of whole-body extracts.²⁶ This might explain the smaller proportion of positive IgE results compared with SPT, even in subjects with a convincing history of an anaphylactic reaction to Argas.

Positive IgE results may be clinically irrelevant, representing only allergic sensitivities without symptoms, which is known for atopic (ie, pollen, mites, animal dander) and Hymenoptera venom allergens. Qualitatively concordant results of SPT and serum IgE to Argas (Table II) indicate an IgE-mediated mechanism in these individuals with a reported bite of Argas. Discordant results between SPT and allergen specific IgE in several subjects (Table II, lower right portion) and poor quantitative agreement (Fig 4) can be attributed to various reasons:

Interestingly, our preliminary study does not provide evidence for an increased risk for atopic individuals of developing an anaphylactic SR after an Argas bite. Similar observations have been reported in subjects being diagnosed for venom hypersensitivity.²⁹ The risk of IgE-mediated clinical reactions to this group of injected allergens is not restricted to atopic individuals, but will also occur in nonatopic subjects. Therefore, allergens from Argas might not be considered atopic allergens, because relevant SRs were more frequently found in subjects without atopic risk.

Atopy, defined by cutaneous sensitivities to common inhalant allergens, seems to influence the test outcome using extracts of Argas, resulting in a higher proportion of positive SPT in this group, similar to diagnostic results in Hymenoptera hypersensitivity.³⁰ Despite displaying an increased risk of allergic sensitization to allergens of Argas, determined by SPT, atopics do not report anaphylactic reactions more frequently than nonatopics. Therefore, diagnostic tests with Argas extracts in atopics should be interpreted with caution, taking into account a higher rate of irrelevant positive SPT results in this group.

Because >80% of the sera from subjects with positive skin reactions to Arg showed IgE-binding to a protein of approximately 22 kd, it might represent a major allergen of Argas. The partial identity of or relationship to a recently described major allergen Arg r 1¹⁸ and to another 22-kd binding protein³¹ remains to be determined. Immunoblot, IgE binding, and inhibition experiments with a rArg r 1–fusion protein indicate that rArg r 1 is recognized by selected sera and that Arg r 1 is also a component of our extract. Considering the salivary origin of mRNA encoding Arg r 1 (see Methods and Results in the Online Repository at www.jacionline.org) and the reactions exclusively occurring after an Argas bite, the most important allergens are likely to be of salivary origin.¹⁴, ¹⁵

In conclusion, we could demonstrate positive SPT and IgE results in subjects with a case history of LRs and/or severe SRs after a bite of the pigeon tick A reflexus. Atopy is a risk factor for positive SPT, but not for SRs, which might occur in some individuals (approximately 8%) after a bite of the soft tick Argas reflexus.

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We thank Dr Dietmar A. Herold and Prof Dr Gert Kunkel (Allergy and Asthma Center Westend, Berlin, Germany) and Martin McCall for editorial assistance and Dr Franziska Rueff (Clinics and OPD of Dermatology, Venerology and Allergology, University of Munich, Germany) for helpful comments on insect related hypersensitivity reactions. Irmgard Löffler, Beate Göhler, Margot Röder, and Vera Passman (Allergy Division of the Clinics and OPD of Dermatology, Venerology and Allergology, University of Leipzig, Germany) provided excellent technical assistance. We acknowledge Dr Ingrid Möller, Dr Sigrun Hillert, and Dr Bodo Gronemann from the local health authorities for administrative support (Gesundheitsamt Stadt Leipzig, Saxony, Germany) and Dr Heide Boysen-Tilly for juristical advice (City of Leipzig, Saxony, Germany). Finally, we thank all participants for their interest in and commitment to the study on pigeon tick allergens. Allergen extract preparation was performed and provided by ALK-Abelló A/S.

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Appendix. Supplementary data 

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