SEARCH

SEARCH BY CITATION

Keywords:

  • birch;
  • familiarity;
  • pollen;
  • pollinosis;
  • ragweed;
  • respiratory allergy

Abstract

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

Background: The effects of sudden and massive exposure of the general population to novel airborne allergens are not known. This study aimed to investigate the clinical effects of two “new” allergens, ragweed and birch, in an area north of Milan during the last 15 years.

Methods:  We reviewed the records of 2571 monosensitized patients seen during the last 10 years in two allergy units north of Milan. Data included age at onset of allergic symptoms, and family history of allergic diseases. In this sample, 500 were allergic to grass, mite, birch, and ragweed; 293 to pellitory; 167 to mugwort; 100 to Alternaria; and 11 to plantain.

Results: Birch pollen-allergic patients and ragweed pollen-allergic patients showed a similar mean age at onset (35.3 years vs. 35.1 years; P = NS), but were significantly older than all other groups of patients (P < 0.001). Patients allergic to ragweed and birch pollen, 304 and 323 respectively, were >30 years at the onset of allergic symptoms. A family history of allergic disorders among first degree relatives was far less frequent among patients allergic to birch pollen (29%) or ragweed pollen (27%) than among patients sensitive to all other airborne allergens, except those allergic to mugwort pollen (P < 0.001). In both ragweed and birch groups, a positive family history was significantly more common among subjects < 30 years than in those > 30 years at onset of respiratory allergy (81/196 (41%) vs. 54/304 (18%), P < 0.001 for the ragweed group; 80/177 [45%]vs. 65/323 (20%), P < 0.001 for the birch group).

Conclusion: Exposure of the general population of this area to two new airborne allergens resulted in the onset of respiratory allergy in many older people who lacked any relevant predisposing factor. Although we cannot exclude the possibility that those who became allergic had been exposed to birch or ragweed pollen elsewhere, a more likely explanation is a specific susceptibility that remains viable until the subject encounters the “right” allergen.

That atopic diseases have a strong genetic basis has been known for many years (1,2). However, genetics studies have been much complicated by variables such as polygenicity, genetic heterogeneity, incomplete penetrance, and by the complex interactions between environmental stimuli and genetic backgrounds. Despite the complex relationship between allergen exposure and sensitization, recent studies have shown a close association between levels of exposure and sensitization to a specific allergen (3). In Western countries, the general population is exposed to both environmental factors that have been shown to facilitate allergic sensitization (4) and to common airborne allergens from early infancy. Consequently, sensitization generally occurs in young people (5).

The concentration of outdoor airborne allergens shows great geographic variability (e.g. pellitory and olive pollen grains are mainly present in Mediterranean areas, birch pollen in Northern countries, ragweed pollen in certain parts of the USA and Europe), which influences the patterns of allergen sensitization observed in different geographic areas.

Little is known about the effects of sudden and massive exposure of the general population in a certain geographic area to airborne allergens that have never been present in that area before; this is exactly what has happened in a suburban area north of Milan. In this area, birch trees became very popular ornamental plants in parks and private gardens during the 1970s and 1980s, causing the appearance of, and a significant increase in, allergic sensitization to tree pollen allergens (6–8). The marked difference in prevalence of birch pollen allergy in people attending allergy clinics in the area north of Milan, compared to those from the city of Milan (5 Km away) where birch trees have not been planted extensively, has been highlighted (9). Even more recently, the whole of the area north of Milan was colonized by short ragweed. The first reports of ragweed allergy in this area appeared in the late 1980s (10,11), and it has gradually become the second most frequent pollinosis in the area (9). The reasons for such a sudden spread of ragweed are still debated. Concentrations of the pollen may reach peaks of > 200 granules/m3. The peak concentrations of birch pollen and ragweed pollen observed in this geographic area during the last few years are summarized in Table 1.

Table 1.  Peak concentrations of birch and ragweed pollen grains 1986–2001 in the area north of Milan
 Pollen counts (number of grains/m3 air)
YearBirchDateRagweedDate
  1. NA = Not available.

1986192Apr 19 48Sep 07
1987350Apr 21 28Sep 07
1988113Apr 13 75Sep 01
1989447Mar 28186Aug 30
1990983Mar 20120Aug 30
1991497Apr 04114Aug 26
1992408Apr 04156Aug 30
1993347Apr 07143Aug 25
1994361Mar 26 50Aug 16
199556Mar 27 69Sep 07
1996249Apr 15198Aug 24
1997321Mar 16119Aug 26
199865Mar 19 96Aug 27
19991650Apr 02 37Aug 25
2000NA 203Aug 27
2001393Mar 30 97Sep 13

This study investigated the effect of the appearance of these “imported” plants by examining the clinical features of patients allergic to “old” and “new” airborne allergens of this area. The study followed the revised nomenclature for allergy of the EAACI (12).

Patients

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

The records of all patients diagnosed with respiratory allergy between 1 January 1990 and 30 September 2001 at the allergy units of two towns 5 km north of Milan (Bollate and Paderno Dugnano) were reviewed. The following clinical data was obtained: age at onset of allergic symptoms (rhinoconjunctivitis and/or asthma); family history of respiratory or food allergy among at least one first-degree relative (one parent and/or one sibling), diagnosed by an allergy center by skin prick test (SPT) and/or radioallergosorbent test (RAST).

Admission criteria

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

To avoid bias caused by overlapping pollen seasons (e.g. grass/pellitory, ragweed/mugwort), by sensitization to crossreacting allergens such as profilin (13,14), or to common allergens in ragweed and mugwort pollen (15) or grass and plantain pollen (16), the study included only monosensitized patients (with a single positive SPT in keeping with the clinical history).

The main airborne allergens in this area were considered. They included grass, pellitory, ragweed, mugwort, plantain, birch, Alternaria, and house-dust mite. The study aimed to investigate the effects of “novel” allergens on the general population, so allergens that only limited numbers of people are exposed to (e.g. cat or dog dander) were not considered. People who are monosensitized to cypress and olive pollen are very rare in the area and were therefore excluded.

Clinical recordings were reviewed in alphabetical order; the maximum number of patients per group was 500.

Skin tests

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

All patients underwent SPT with a standard panel of commercial extracts (Allergopharma; Reinbeck, Germany) of airborne allergens including: grass, mugwort, ragweed, pellitory, plantain, birch, cypress, olive, Alternaria, house dust mite, cat dander, and dog dander. Skin tests were carried out and read following established methods (17).

Statistics

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

Means were compared by the two-tailed Student's t-test. Proportions were compared by chi-squared test with Yates' correction. Probability values less than 5% were considered significant.

Results

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

A total of 2571 patients (500 allergic to grass, mite, birch, and ragweed; 293 to pellitory, 167 to mugwort, 100 to Alternaria, and 11 to plantain) were studied. Results are shown in Table 2. Birch pollen- and ragweed pollen-allergic patients had a similar mean age at onset (35.3 years vs. 35.1 years; P = NS), but were significantly older than all the other groups (P < 0.001). The age at onset of allergic symptoms showed a nearly normal distribution in both ragweed pollen- and birch pollen-allergic patients, whereas in all other groups the distribution was markedly skewed towards younger ages (Table 3). Patients allergic to ragweed and birch pollen > 30 years old at the onset of respiratory allergy were 304 and 323 respectively.

Table 2.  Age at onset of respiratory symptoms and family history in 2571 monosensitized allergic patients
AllergenNo. patientsAge at onset (years)Family history
Mean (SD)RangeMedian
  • *

    P  < 0.001.

Birch50035.3 (13.3)* 3–713529%*
Ragweed50035.1 (12.4)* 5–763327%*
Grass50018.6 (9.8) 2–581747%
Mite50018.4 (11.3) 2–731646%
Pellitory29326.2 (11.6) 3–662545%
Mugwort16727.4 (11.9) 8–692531%*
Alternaria10015.1 (8.1) 2–401351%
Plantain 1122.5 (7.2)12–322644%
Table 3.  Distribution of 2571 monosensitized patients with respiratory allergy by age and allergen
 Age at onset (years); number (%)
Allergen0–1516–3031–4546–60> 60
Birch 38 (8%)139 (28%)215 (43%)87 (17%)21 (4%)
Ragweed 22 (4%)174 (35%)209 (42%)78 (16%)17 (3%)
Grass216 (43%)224 (45%) 53 (11%) 7 (1%) 0 (0%)
Mite240 (48%)194 (39%) 47 (9%)16 (3%) 3 (1%)
Pellitory 48 (16%)165 (56%) 65 (22%)13 (4%) 2 (1%)
Mugwort 20 (12%) 93 (56%) 38 (23%)13 (8%) 3 (2%)
Alternaria 54 (54%) 40 (40%)  6 (5%) 0 (0%) 0 (0%)
Plantain  3 (30%)  7 (60%)  1 (10%) 0 (0%) 0 (0%)

A family history of allergic disorders among first degree relatives was significantly less frequent for patients allergic to birch pollen (29%) or ragweed pollen (27%) than among those sensitive to all other airborne allergens except those allergic to mugwort pollen (P < 0.001; Table 2). In both ragweed- and birch- hypersensitive groups, a positive family history was significantly more common among those aged < 30 years than those aged > 30 years (81/196 (41%) vs. 54/304 (18%), P < 0.001 for the ragweed group; 80/177 (45%) vs. 65/323 (20%), P < 0.001 for the birch group). The subgroups did not show any relevant difference in the clinical features of respiratory allergy (asthma and/or rhinoconjunctivitis) at onset.

Discussion

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

It is well known that most patients develop respiratory allergy before the age of 20, and that initial symptoms appear only occasionally in middle to old age (5). The observation that allergy to pellitory pollen appears some years later than allergy to grass pollen is not surprising (8); but the finding, that in this area the average age of onset for both birch and ragweed allergy is 35 years, was unexpected. Interestingly, ragweed-allergic people were significantly older than those allergic to mugwort (a member of the Compositae family, sharing some minor allergens with ragweed, which has always been in this area). There is some possibility that the later age of onset for birch and ragweed allergy relates to the fact that older people have traveled more widely, perhaps being exposed to these allergens elsewhere. A more reasonable explanation for these findings, however, could be a strictly specific genetic predisposition of some people for developing respiratory allergy.

Both ragweed pollen- and birch pollen-allergic subjects in this area have spent their whole lives in contact with mites, moulds, grass, pellitory and mugwort pollens, and most of them had never traveled abroad, but they became allergic at older ages, only after being exposed for long enough to the “new” allergens. It is tempting to speculate that if these people had lived in areas where both birch trees and ragweed were not present, they would not have developed any respiratory allergy. Such speculation would also suggest that, in general, a genetic predisposition to allergic disease is more common than believed, and that many people do not develop clinically relevant respiratory allergies simply because they have not been exposed to the “right” specific allergen(s) for long enough. An alternative explanation may be that exposure to high levels of a “new” allergen induces sensitization also in people with a low disposition for atopy. In previous studies, adult immigrants from Asia and Turkey developed birch pollen allergy after spending a few years in Sweden, and the prevalence of this allergy was related to the time spent in Sweden (18). Similarly, the introduction of blankets in Papua New Guinea was associated with a 70-fold increase of asthma (19). The immigrant model is characterized by exposure to a native allergen that has been stable for a long time and by subsequent sensitization within a few years. However, this model might not fit well the situation described here, with concentrations of birch and ragweed pollen probably increasing over many years.

The family histories were also interesting. Possibly the results were influenced by the exclusion of people with multiple hypersensitivities to airborne allergens (a subset that is more likely to develop respiratory allergy at a young age and to show a family history of allergic diseases). However, a family history of atopic disorders was significantly less frequent in both birch and ragweed pollen-allergic patients than in most other groups. Surprisingly, in younger patients the prevalence of a positive family history did not differ from that observed in most of the other groups.

In conclusion, this study shows that exposure of the population living in this area to two new airborne allergens resulted in the onset of respiratory allergies in older people who seemed to lack relevant predisposing factors. The existence of a specific susceptibility that remains viable until the “right” allergen is encountered cannot be excluded.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References

The author thanks Dr Giuseppe Albasser, Divisione di Medicina II, Allergologia, Ospedale di Gallarate for providing the pollen concentrations data.

References

  1. Top of page
  2. Abstract
  3. Material and methods
  4. Patients
  5. Admission criteria
  6. Skin tests
  7. Statistics
  8. Results
  9. Discussion
  10. Acknowledgments
  11. References
  • 1
    Cooke RA, Van Der V eer A. Human sensitization. J Immunol 1916;1:201305.
  • 2
    Hopp RJ, Bewtra AK, Watt GD. Genetic analysis of allergic disease in twins. J Allergy Clin Immunol 1984;73:265270.
  • 3
    Murray CS, Woodcock A, Custovic A. The role of indoor allergen exposure in the development of sensitization and asthma. Curr Opin Allergy Clin Immunol 2001;1:407412.
  • 4
    Liccardi G, Custovic A, Cazzola A, Russo M, D'Amato M, D'Amato G. Avoidance of allergens and air pollutants in respiratory allergy. Allergy 2001;56:705722.
  • 5
    Evans R. In Middleton E, Reed CE, Ellis EF, Adkinson NF, Yuninger JW, Busse, WW, editors. Allergy. Principles and Practice, 4th edn. St. Louis, MO: Mosby 1993, 11091136.
  • 6
    Dal Bo S, Dal Bo GA. La pollinosi da Betulla e da Betulaceae. Giorn It Allergol Immunol Clin 1991;1:475478.
  • 7
    Ortolani C, Fontana A, Bosetti M, Ciccarelli M. Pollinosi in Lombardia. Giorn It Allergol Immunol Clin 1991; 1:515518.
  • 8
    D'Amato G, Spieksma FThM, Liccardi G, Jager S, et al. Pollen-related allergy in Europe. Allergy 1998;53:567578.
  • 9
    Asero R, Qualizza R, Schilke ML, Sillano V, Zanoletti T. Studio multicentrico sulla prevalenza delle pollinosi nella città e nella provincia di Milano: 1990–95. Giorn It Allergol Immunol Clin 1998;8:241 (abstract).
  • 10
    Piazza G, Cassani L, Sesia O, Corti M, Della Torre F. Ragweed evidence in a North Milan hill area. International Symposium: Pollinosis in the Mediterranean area. Naples, March 16–18 1989, 197 (abstract).
  • 11
    Bottero P, Venegoni E, Riccio G, et al. Pollinosi da Ambrosia artemisiifolia in provincia di Milano. Folia Allergol Immunol Clin 1990;37:99103.
  • 12
    Johansson SGO, Hourihane JO'B, Bousquet J, et al. A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 2001;56:813824.
  • 13
    Van Ree R, Voitenko V, Van L eeuwen WA, Aalberse RC. Profilin is a cross-reactive allergen in pollen and vegetable foods. Int Arch Allergy Immunol 1992;98:97104.
  • 14
    Valenta R, Duchene M, Ebner C, et al. Profilins constitute a novel family of functional plant pan-allergens. J Exp Med 1992;175:377385.
  • 15
    Hirschwehr R, Heppner C, Spitzauer S, Sperr W, et al. Identification of common allergenic structures in mugwort and ragweed pollen. J Allergy Clin Immunol 1998;101:196206.
  • 16
    Asero R, Mistrello G, Roncarolo D, Casarini M. Detection of allergens in plantain (Plantago lanceolata) Pollen Allergy 2000;35:10591062.
  • 17
    Bousquet J, Michel FB. In Middleton E, Reed CE, Ellis EF, Adkinson NF, Yunginger YJ, Busse WW, editors. Allergy. Principles and Practice, 4th edn. St. Louis, MO: Mosby 1993, 573594.
  • 18
    Kalyoncu A, Stalenheim G. Serum IgE levels and allergic spectra in immigrants to Sweden. Allergy 1992;47:277280.
  • 19
    Dowse GK, Turner KJ, Stewart GA, Alpers MP, Woolcock AJ. The association between Dermatophagoides mites and the increasing prevalence of asthma in village communities within the Papua New Guinea highlands. J Allergy Clin Immunol 1985;75:7583.