Original Article Atopic disease presentation in northeastern China: a 10-year retrospective study
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Int J Clin Exp Med 2016;9(2):2067-2075
www.ijcem.com /ISSN:1940-5901/IJCEM0012735
Original Article
Atopic disease presentation in northeastern
China: a 10-year retrospective study
Hua Xie1, Wei-Wei Song1, Ruo-Nan Chai1, Shao-Heng He2
1
Center for Allergy and Immunotherapy, General Hospital of Shenyang Military Area Command, Shenyang
110840, China; 2Center for Allergy and Clinical Immunology, The First Affiliated Hospital of Liaoning Medical
University, Jinzhou 121001, China
Received July 11, 2015; Accepted November 19, 2015; Epub February 15, 2016; Published February 29, 2016
Abstract: This study was designed to investigate the prevalence pattern and characteristics of atopic disease in
patients in the second largest allergy clinic in China. All clinical data associated with 103,370 patients treated
at our allergy clinic between January 2001 and December 2010 were analyzed. There was a 3.4-fold increase in
allergy cases over this 10-year period, with significant increases in hospital visits associated with asthma (43%),
rhinitis (31.6%), and urticaria (11.7%), in particular. The highest incidence rates occurred in August, followed by
September, and then July. Of 57,887 positive SPT (skin prick test) patients (positive rate of 56%), the main allergens
identified were Dermatophagoides pteronyssinus (77.8%), D. farinae (75.1%), Artemisia vulgaris (40.5%), Ambrosia
elatior (22.3%), dog dander (10.9%), and Humulus scandens (1.9%). About 65.5% (22,253/33,974) of SPT positive
patients responded to at least one type of allergen in serum specific IgE (sIgE) tests. Approximately 18.2% of the pa-
tients seen were tested for sIgE reactivity for differential diagnosis purposes although they did not exhibit any signs
of atopic disease. Our observations provide allergists with current data for patients in China, which will improve
prevention, diagnosis, and treatment of atopic diseases.
Keywords: Allergens, northeastern China, incidence rate, skin prick test, sIgE test
Introduction increased from 8.5% in 1996 to 13.3% in 2005
[4], and in Brazil, the prevalence of asthma in
A 2004 World Allergy Organization’s (WAO’s) children increased at an annual rate of 1% dur-
Specialty and Training Council survey of WAO’s ing the decade of 1998 through 2008 [5].
33 member societies conducted to obtain These relatively focused regional data are con-
information regarding allergy rates worldwide sistent with the aforementioned WAO conclu-
indicated that approximately 22% of the sur- sion that atopic disease incidence rates are
veyed populations suffered from some form of increasing steadily. Because China does not yet
allergic disease [1]. Their observations belie an have a nationwide allergy prevalence survey, we
apparent dramatic increase in the prevalence set out to establish allergy incidence rates at
of allergic diseases in both developed and our hospital, located in northeastern China,
developing countries. Increasing prevalence where an allergy clinic has been active since
rates of allergic diseases place a significant 1964.
burden on health care systems worldwide.
A relationship between increased rates of chil-
A large regional study indicated that the preva- dren presenting at emergency departments for
lence of asthma symptoms in children living in asthma and seasonal increases in ambient
Western Europe (57 centers in 12 countries) grass pollen levels has been observed, with a
increased by 2.7% between 1992 and 1996 pollen level threshold as low as 19 grains/m3
[2]. In England, cases of allergic rhinitis in- [6]. In addition, the incidence of cases of acute
creased by 43.2% between 2001 and 2005 urticaria (AU) presenting to emergency depart-
[3]. In Ontario, Canada, asthma prevalence ments in Norwich (UK) and Heraklion (Crete,Atopic diseases in northern China
Greece) have been reported to be inversely respondence, in a single targeted hospital in
associated with temperature. A non-significant northeastern China.
seasonal pattern of AU incidence (October,
April-May) was observed in Norwich, in contrast Materials and methods
to the significant seasonal pattern (December,
February-May) of AU described for Heraklion Subjects
[7]. However, a regression analysis failed to
At the end of 2011, we analyzed patient data
identify a significant relationship between aver-
collected at the Center for Allergy and Immu-
age annual temperatures and the prevalence of
notherapy in the General Hospital of Shenyang
hay fever in the National Health Interview
(Liaoning Province, China)-the second largest
Survey conducted in the USA [8], suggesting
allergy clinic in China-from January 2001 th-
that seasonal climate changes play a compli-
rough December 2010 (the decade following
cated role in the presentation of allergic disea-
the clinic’s 2011 conversion to an electronic
ses.
patient database). Following doctor visits, infor-
Furthermore, comparing data across different mation regarding diagnostic test results and
countries suggests that the prevalence of atop- diagnosis was added to the database. Diagnosis
ic diseases differs greatly between regions. For and grouping criteria for asthma and allergic
example, the prevalence of asthma, eczema, rhinitis were conducted according to the Gui-
and hay fever among Ethiopian women in 2005- delines for the Prevention and Treatment of
2006 was reported to be 1.7%, 0.9% and 3.8%, Asthma published by the Chinese Medical
respectively [9]. Meanwhile, symptoms sugges- Association in 1997 and 2003 and the Gui-
tive of a history of asthma, eczema, and rhinitis delines for the Diagnosis and Treatment of
were observed in 23.6%, 10.3% and 24.2% of Allergic Rhinitis published by the Chinese
children examined in a study in Madinah, Saudi Medical Association in 1997 and 2005. The
Arabia [10]. study was approved by the ethical committee of
the General Hospital of Shenyang Military Area
It has been reported that the most common Command (No: K18 of 2000).
allergens causing sensitization in southern
India are house-dust mite allergens (range, SPT and sIgE tests
65-70%), tree pollens (range, 52-56%), and
Contraindications for SPTs were use of antihis-
cockroach antigens (range, 39-53%) [11]. In
tamines, steroids, or other drugs within the last
China, overall prevalence of positive skin prick
2 weeks, symptoms of dermatographia, and
test (SPT) responses have been reported to be
active skin disorders. The tests were performed
59.0% for Dermatophagoides farina (a dust
according to standard methods with a panel of
mite), 57.6% for D. pteronyssinus (a dust mite),
inhaled common allergens (ALK, Denmark) and
40.7% for Blomia tropicalis, 16.1% for American
food allergens. Histamine dihydrogen chloride
cockroach antigens, 14.0% for dog allergens,
and 1% glycerinate solution served as positive
11.5% for Blatella germanica, 11.3% for
and negative controls, respectively. SPTs were
Artemisia vulgaris, 10.3% for cat dander, 6.5%
read 15 min after antigen administration and a
for Ambrosia artemisifolia, 3.5% for mixed
weal that was at least 3 mm larger than the
grass pollen, and 2.2% for mixed tree pollen negative control was considered positive. sIgE
[12]. Undoubtedly, these broad-area surveys tests were performed with the UniCAP system
are important for understanding the regional and commercial reagent kits (Pharmacia Diag-
prevalence of allergies, but they do not provide nostics AB, Uppsala, Sweden) in accordance
reliable information about the incidence and with the manufacturer’s instructions.
characteristics of allergy symptoms in patients
at any given hospital within the large regions Statistical analysis
surveyed. Furthermore, the correspondence
between SPT results and serum allergen-spe- Simple descriptive statistics, conducted in
cific immunoglobulin-E (sIgE) test results is SPSS 17 software, were used to analyze patient
unclear. Hence, the aim of the current study characteristics. The prevalence rates for spe-
was to analyze atopic disease incidence data cific allergic diseases were calculated by divid-
collected over 10 years, including SPT-sIgE cor- ing the number of cases by the total number of
2068 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern Chin
years, 14-30 years, 30-60
years, and >60 age bands
were 31,321 (30.3%), 20,881
(20.2%), 34,836 (33.7%), and
16,332 (15.8%), respectively.
The number of allergy patient
visits to our clinic in 2010 was
3.4-fold greater than that
observed in 2001. However, a
steady ascending year-over-
year curve was not observed
for the entire decade. Rather,
following a generally increas-
ing trendline for 8 years, the
number of the allergic patients
in our clinic then appeared to
decrease over the last 2 years
of the decade (Figure 1A). As
shown in Figure 1B, apart
from patients being seen for
asthma and rhinitis, the per-
centage of first-visit patients
at the clinic exceeded that of
subsequent-visit patients. In
Figure 1. A. Annual allergy clinic visits. The number of patients who visited
particular, patients with acute
our allergy clinic in Shenyang, China during each year from 2001 through drug or food allergies were
2010 is shown. B. New versus return patients. The relative portions of allergy unlikely to return to the clinic
clinic visits involving new patients (first visits) and return patients (subse- for a second visit.
quent visits) in the study period.
Types of allergic diseases
outpatients visiting the clinic during the same It has long been recognized that allergic rhini-
time period. Nonparametric nominal data were tis, asthma, and urticaria represent the three
compared between groups with the rank sum major clinical allergic diseases. However, it
test of two independent samples and expressed seems likely that the ratio between each of
as medians and ranges. Parametric data were these varies between populations. For instance,
analyzed with the Chi-square test and ex- the prevalence of asthma, eczema, and hay
pressed as percentages. P values < 0.05 were fever was 1.7%, 0.9% and 3.8%, respectively, in
considered statistically significant. an Ethiopian population [9], but in Madinah,
Saudi Arabia the rates respectively were 23.6%,
Results 10.3% and 24.2% [10].
Patient demographics Asthma (N = 44,492, 43.04%), rhinitis (N =
32,670, 31.60%), and urticaria (N = 12,065,
A relatively steady trend of increasing allergy 11.67%) were the three most common atopic
incidence has been observed worldwide, and diseases observed in patients in our clinic.
as much as a 1% annual increase in the num- Together, these three diseases accounted for
ber of allergic patients have been reported [5]. 86.3% (N = 89,227) of all patient visits to the
As a result we anticipated similar results in our clinic (Table 1). A detailed profile of the disease
patient population. diagnoses of our patients by year is shown in
Figure 2.
Complete data were available for 103,370 cli-
nic visits. Of these 103,370 visits examined, Seasonal distribution
54,121 involved male patients and 49,249
involved female patients (ratio of l.1:1). The A non-significant seasonal trend in AU inci-
numbers of visits in which patients in the < 14 dence (October, April-May) was observed in
2069 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern China
Table 1. Allergic diseases diagnosed in our dander (4,920 cases, 8.5%), tree pollen (2,373
hospital allergy clinic in Shenyang, China, cases, 4.1%), and H. scandens (1,099 cases,
2001-2010 1.9%) (Table 2).
Percentage of
Disease Number SPT versus serum sIgE tests
total cases
Asthma 44,492 43.04 A previous study of 138 school children (age
Rhinitis 32,670 31.60 6-8 years) showed that the majority of subjects
Urticaria 12,065 11.67 with positive SPT reactions to respective aller-
Dermatitis 3,541 3.43 gens also had increased sIgE levels. A signifi-
Eczema 3,377 3.27 cant correlation between the SPT and sIgE lev-
Purpura 1,989 1.92 els was found for Dpt, birch pollens, and grass
Conjunctivitis 919 0.89 pollens [13]. It was also demonstrated that
Nerve vasculitis 619 0.60 98% of 104 patients with allergic rhinoconjunc-
tivitis presented with a positive skin test reac-
Drug allergy 367 0.36
tion that correlated with the presence of sIgE
Food allergy 159 0.15
specific for timothy grass pollen [14].
Nervous headaches 149 0.14
Allergic colitis 75 0.07 However, the relationship between clinical ma-
Other 2,948 2.85 nifestations and SPT (or sIgE) in a large scale
Total 103,370 100.00 remains unclear.
About a third of the 103,370 patients (N =
Norwich, in contrast to a significant seasonal 33,974; 32.9%), constituting a majority (58.7%)
impact (December, February-May) of AU des- of the 57,887 patients with positive SPT res-
cribed in Heraklion [7], suggesting that the ponses, had corresponding sIgE responses to
influence of climate on allergic disease presen- allergens in our analysis. About two thirds of
tation varies between geographic areas. the patients with sIgE responses (22,253/
33,974; 65.5%) showed a positive SPT response
A summary of allergy patients visits to our cli- to at least one allergen.
nic by month is shown in Figure 3. The high-
est numbers of patients sought treatment in The number of patients with positive SPT and
August, followed by September and July. Ja- positive serum sIgE test results for particular
nuary and February had the fewest patient allergens are reported in Table 2 together with
seen. In particular, patients presenting with the portion of SPT-positive patients who also
asthma increased between July and September, had corresponding positive serum sIgE test
and peaked in August. Rhinitis cases also results for particular allergens. Notably, only
peaked in August, and decreased between May 17.5% of the patients with positive D. farina
and July. Urticaria cases started to increase in SPT results also showed corresponding posi-
June and peaked in September. tive sIgE results. Meanwhile, 46.4% of the
patients with positive H. scandens SPT results
Identification of allergens using the SPT also showed corresponding sIgE results. The
numbers of the patients with positive sIgE
SPT is a common and relatively reliable means results varied from year to year. Generally
for determining allergic responses to specific speaking, many more patients with positive
allergens. sIgE results were observed in 2005 and 2010
than in 2001. Notably, H. scandens represent-
Among the 103,370 patient visits for which ed a novel allergen in 2005 and a surge of
cases files were examined in this study, 57,887 patients with positive sIgE against H. scandens
(56%) yielded a positive SPT result. The main was observed in 2010 (Figure 4A).
allergens eliciting positive SPT results were
dust mite allergens (D. pteronyssinus, 45,036 Clinical diseases associated with positive se-
cases, 77.8%; and D. farinae 43,473 cases, rum sIgE results
75.1%), Artemisia vulgaris (23,444 cases,
40.5%), Ambrosia elatior (12,908 cases, Based on the current definition of allergy, a
22.3%), dog dander (6,310 cases, 10.9%), cat group of diseases largely driven by IgE mediat-
2070 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern Chin
Figure 2. Disease profiles of patients diag-
nosed at the clinic between 2001 and 2010.
ed mechanisms [15], sIgE tests play a pivotal use sIgE tests in patients without atopic dis-
role in the diagnosis of allergy, particularly in eases. The percentage of patients presenting
the identification of specific allergens resulting with particular diseases who were subjected to
in the presentation of respective atopic diseas- serum sIgE tests are summarized in Figure 4B.
es. Since allergy symptoms are not unique to Approximately 18.2% of non-allergy patients
allergic diseases, clinicians could mistakenly seen during the study period were submitted to
2071 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern China
Regional differences may be
due, at least in part, to the
fact that our analysis included
both first and second visits.
Thus, some of the cases in-
cluded in our analysis were
not new cases. In addition,
Chinese patients tend to visit
large regional hospitals or
clinics straight away without
visiting local district clinics
first.
Allergic manifestations requir-
ing subsequent visits to the
Figure 3. Variation in monthly outpatient visits. Odds ratios of allergic dis-
clinic varied. For example,
ease relative to the number of cases seen in January are shown.
subsequent visits for asthma
or rhinitis were more frequent
Table 2. Summary and relation of positive since standardized treatments for asthma and
skin prick test (SPT) and specific IgE (sIgE) rhinitis require regular scheduled follow-up vis-
test results its. In contrast, most patients with food and
Specific allergen Positive Positive Positive drug allergy were less likely to return the clinic
source SPT sIgE sIgE/SPT for further treatment.
D. pteronyssinus 45036 11580 0.257128 Patients with and without atopic disease visit-
D. farinae 43473 7600 0.174821 ed our clinic because some allergic diseases
Artemisia vulgaris 23444 6900 0.294318 are difficult to differentiate from other illnesses
Ambrosia elatior 12908 2360 0.182832 based only on clinical symptoms. To our knowl-
Dog dander 6310 2840 0.450079 edge, this is the first report describing visits of
Cat dander 4920 1270 0.258130 non-allergy patients to an allergy clinic in China.
Tree pollen 2373 780 0.328698 Although variations on the types of allergic
diseases observed varied from year to year
Humulus scandens 1099 510 0.464058
over the 10-year period analyzed, asthma and
D. pteronyssinus = Dermatophagoides pteronyssinus, D.
farina = Dermatophagoides farina.
allergic rhinitis were consistently the two most
commonly observed atopic diseases observed
throughout the study. Skin allergy cases were
serum sIgE tests for differential diagnosis pur- relatively low, likely due to some skin allergy
poses. patients being treated by the dermatology
department.
Discussion
Data provided in this report may help others
In the present study, we observed an upward understand the numbers and varieties of atop-
trend in allergy case visits between 2001 and ic diseases presenting in northern China.
2010. Specifically, we observed a 3.4-fold Demographically, the 30-60-year age band
increase in allergy clinic visits over this 10-year group exhibited the highest allergy rates. This
period, which indicates that the increase in our observation is consistent with a previous study
area far exceeds increases seen elsewhere, reporting that the prevalence of positive SPTs
such as the 1% yearly increase reported in and mean total serum IgE levels in asthmatics
Brazil [5]. The upward trend in visits can be did not decline with advancing age in California
attributed to a roughly steady increase in the [16]. Further consistent with this result is the
first 8 years of the decade, followed year-over- finding that the age of adult-onset asthma
year reductions for the last 2 years. The rea- appears to be increasing among females in
sons for the decreased hospital visit rates Japan [17].
observed at our clinic in the last couple years of
the study period are not known. However, it The increases in clinic visits over the summer
should be noted that the decrease was certain- months may be attributable to similarly timed
ly not due to limited capacity. zeniths in the grass pollen and fungi seasons.
2072 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern Chin
positive SPT responses in our
clinic were from D. pteronys-
sinus, D. farinae, Artemisia
vulgaris, Ambrosia elatior,
and dog dander. Tree pollen
was only responsible for 4.1%
of atopy cases, which is not
sufficient to have caused the
major rise in allergy cases
observed between July and
September. Given that the top
two allergen sources among
our studied population were
two dust mite species, surges
in dust mite populations may
underlie the summer increas-
es in allergy visits. A prior
study of dust mite allergen
concentrations in beds indi-
cated that these allergens
peak in late autumn in Sydney
[20]. In addition, a study in
Turkey showed that sensitiza-
tion to pollens, house dust,
and molds was 59.7%, 20.5%
and 2%, respectively, and that
grass pollen sensitivity was
3-fold more common than
tree pollen allergies [21], sup-
porting our observation that
the major rise in allergy cases
Figure 4. A. Numbers of patients with positive sIgE results in 2001, 2005, occurred in autumn.
and 2010. Serum sIgEs against a panel of allergens were measured. d1
= Dermatophagoides pteronyssinus; d2 = Dermatophagoides farina; w6 = It should be noted that a
Artemisia vulgaris; w1 = Ambrosia elatior; w22 = Humulus scandens. B. severe IgE-mediated respon-
Clinical diseases associated with sIgE tests. The data were presented as the
se to aeroallergens and air-
percentage of total sIgE measured.
way inflammation could acco-
unt for the increasing preva-
Researchers in Ecuador observed a similar lence of allergic respiratory diseases in pollut-
allergy peak in August [19]. Notwithstanding, ed urban areas. The most abundant compo-
allergy case trends do not always follow envi- nents of urban air pollution in urban areas with
ronmental allergen trends. For example, it is high levels of vehicle traffic are airborne partic-
unclear why visits from patients with urticaria ulate matter, nitrogen dioxide, and ozone [22].
in our study peaked in September. In this
regard, in 1956, Kaufmann and Mayer [18] The correlation between SPT and sIgE results
observed a surprising dissociation between has been variable across studies. Most studies
allergy clinic visits and tree pollen peaks. have involved relatively small populations of
perhaps several hundred subjects. In our large
Determination of what allergens are responsi- sample, only 65.5% of SPT-positive patients
ble for atopic disease presentation is critical for had corresponding sIgE results. The correspon-
the development of efficacious treatment plans dence was particularly poor for D. farina aller-
for allergic disease patients. Using standard- gens (only 17.5%), and moderately better for H.
ized protocols for the identification of allergens, scandens allergens (46.4%). Better SPT/IgE
we found that the top five allergens eliciting correspondence has been reported in smaller
2073 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern China
studies. For example, Schuetze et al. found that in our area may be a key to elucidating the cur-
a majority of 138 children (age, 6-8 years) with rent landscape of allergens in our region.
positive SPT reactions to specific allergens had
corresponding increased sIgE responses [13]. Acknowledgements
In a study of 104 allergic rhinoconjunctivitis
patients with positive SPT reactions, Huss- The authors are grateful for the excellent tech-
Marp et al. also observed good correlation nical support provided by Zhi-Hui Lv, Xiao-Juan
(98%) with sIgE reactivity for timothy grass pol- Feng, and Chun-Feng Xu. This project was spon-
len, although a dose-response relationship be- sored by the grants from the Natural Science
tween sIgE level and clinical outcome of timo- Foundation of Liaoning Province, China (2012-
thy allergen exposure could not be established 02244), the National Natural Science Found-
[14]. Conversely, poor relationships between ation of China (No. 81172836) Clinical Capa-
SPT and sIgE results have been described for bility Construction Project for Liaoning Pro-
children with dairy allergens, regardless of vincial Hospitals (LNCCC-A06-2014), and “12th
whether the children presented with the rele- five-year” public welfare industry special scien-
vant food allergies [23]. tific research project (201502012).
The yearly shifting trend of positive serum sIgEs Disclosure of conflict of interest
against novel allergens such as H. scandens in
our area is of interest because it is reasonable None.
to expect that people will encounter more nov-
Address correspondence to: Hua Xie, Center for
el allergens over time. Given this expectation,
Allergy and Immunotherapy, General Hospital of
efforts need to be made to better understand
Shenyang Military Area Command, No. 83, Wenhua
environmental allergen patterns, particularly
Road, Shenhe Distric, Shenyang 110840, China. Tel:
with respect to the presentation of atopic dis-
+86-24-23890592; Fax: +86-24-23890592; E-mail:
eases in the industrialized world.
13309885483@163.com; Shao-Heng He, Center
Although 33,974 patients were given sIgE tests for Allergy and Clinical Immunology, The First
in our clinic over the 10-year period examined, Affiliated Hospital of Liaoning Medical College, No.
we are still not sure which atopic diseases 2, Section 5, Renmin Road, Jinzhou 121001, China.
should be screened in this manner due to the Tel: +86-416-4167077; Fax: +86-416-4167426;
cost of the test and the variability of results. For E-mail: shoahenghe@hotmail.com
example, 77%, 94%, and 68% of Finnish chil-
References
dren, and 43%, 67%, and 41% of Russian chil-
dren with asthma, hay fever, and eczema, [1] Warner JO, Kaliner MA, Crisci CD, Del Giacco S,
respectively, were found to be sIgE positive in Frew AJ, Liu GH, Maspero J, Moon HB,
the same study [24]. Our results with sIgE tests Nakagawa T, Potter PC, Rosenwasser LJ, Singh
may provide a useful guide for allergists given AB, Valovirta E, Van Cauwenberge P. Allergy
that this is the first large scale study describing practice worldwide: a report by the World
the use of these tests. Allergy Organization Specialty and Training
Council. Int Arch Allergy Immunol 2006; 139:
In conclusion, we analyzed data collected over 166-174.
a 10-year period at the second largest allergy [2] Weiland SK, Husing A, Strachan DP, Rzehak P,
clinic in China. To our knowledge, this is one of Pearce N, Group IPOS. Climate and the preva-
only a few large-scale studies conducted at a lence of symptoms of asthma, allergic rhinitis,
single allergy clinic. This study provides a host and atopic eczema in children. Occup Environ
Med 2004; 61: 609-615.
of useful datasets for clinicians, researchers,
[3] Ghouri N, Hippisley-Cox J, Newton J, Sheikh A.
and patients, including a 3.4-fold increase in
Trends in the epidemiology and prescribing of
annual allergy case visits over a 10-year period, medication for allergic rhinitis in England. J R
monthly clinic visitation patterns, and allergy Soc Med 2008; 101: 466-472.
incidence seasonality, and identifies the top [4] Gershon AS, Guan J, Wang C, To T. Trends in
allergens associated with atopic disease in our asthma prevalence and incidence in Ontario,
area. Moreover, our observation that H. scan- Canada, 1996-2005: a population study. Am J
dens represents an emergent allergen source Epidemiol 2010; 172: 728-736.
2074 Int J Clin Exp Med 2016;9(2):2067-2075Atopic diseases in northern Chin
[5] Wehrmeister FC, Menezes AM, Cascaes AM, [15] Adkinson NFJ, Bochner BS, Busse WW, Holgate
Martinez-Mesa J, Barros AJ. Time trend of asth- ST, Lemanske RFJ, Simons FER. Middleton’s
ma in children and adolescents in Brazil, Allergy, Principles and Practice Edition 7. Mos-
1998-2008. Rev Saude Publica 2012; 46: by Elsevier; 2009.
242-250. [16] Crawford WW, Gowda VC, Klaustermeyer WB.
[6] Erbas B, Akram M, Dharmage SC, Tham R, Age effects on objective measures of atopy in
Dennekamp M, Newbigin E, Taylor P, Tang ML, adult asthma and rhinitis. Allergy Asthma Proc
Abramson MJ. The role of seasonal grass pol- 2004; 25: 175-179.
len on childhood asthma emergency depart- [17] Tsukioka K, Toyabe S, Kogusuri Y, Akazawa K.
ment presentations. Clin Exp Allergy 2012; 42: The age of onset of adult-onset asthma is in-
799-805. creasing in Japanese women. Arerugi 2009;
[7] Konstantinou GN, Papadopoulos NG, Tavladaki 58: 1591-1601.
T, Tsekoura T, Tsilimigaki A, Grattan CE. Child- [18] Kaufmann M, Mayer LD. Seasonal allergy. J Ky
hood acute urticaria in northern and southern State Med Assoc 1956; 54: 137-144.
Europe shows a similar epidemiological pat- [19] Valdivieso R, Iraloa V. Monthly variation of
tern and significant meteorological influences. Dermatophagoides allergens and its influence
Pediatr Allergy Immunol 2011; 22: 36-42. on respiratory allergy in a high altitude environ-
[8] Bhattacharyya N. Does annual temperature in- ment (Quito, 2800 m a.s.l. in Andean Ecuador).
fluence the prevalence of otolaryngologic re- Allergol Immunopathol (Madr) 2011; 39: 10-
spiratory diseases? Laryngoscope 2009; 119: 16.
1882-1886. [20] Crisafulli D, Almqvist C, Marks G, Tovey E.
[9] Amberbir A, Medhin G, Hanlon C, Britton J, Seasonal trends in house dust mite allergen in
Venn A, Davey G. Frequent use of paracetamol children’s beds over a 7-year period. Allergy
and risk of allergic disease among women in 2007; 62: 1394-1400.
an Ethiopian population. PLoS One 2011; 6: [21] Erel F, Karaayvaz M, Caliskaner Z, Ozanguc N.
e22551. The allergen spectrum in Turkey and the rela-
[10] Nahhas M, Bhopal R, Anandan C, Elton R, tionships between allergens and age, sex,
Sheikh A. Prevalence of allergic disorders am- birth month, birthplace, blood groups and fam-
ong primary school-aged children in Madinah, ily history of atopy. J Investig Allergol Clin Im-
Saudi Arabia: two-stage cross-sectional survey. munol 1998; 8: 226-233.
PLoS One 2012; 7: e36848. [22] D’Amato G, Cecchi L, D’Amato M, Liccardi G.
[11] Mahesh PA, Kummeling I, Amrutha DH, Urban air pollution and climate change as envi-
Vedanthan PK. Effect of area of residence on ronmental risk factors of respiratory allergy: an
patterns of aeroallergen sensitization in atopic update. J Investig Allergol Clin Immunol 2010;
patients. Am J Rhinol Allergy 2010; 24: e98- 20: 95-102; quiz following 102.
103. [23] Mehl A, Niggemann B, Keil T, Wahn U, Beyer K.
[12] Li J, Sun B, Huang Y, Lin X, Zhao D, Tan G, Wu Skin prick test and specific serum IgE in the
J, Zhao H, Cao L, Zhong N, China Alliance of diagnostic evaluation of suspected cow’s milk
Research on Respiratory Allergic D. A multicen- and hen’s egg allergy in children: does one re-
tre study assessing the prevalence of sensiti- place the other? Clin Exp Allergy 2012; 42:
zations in patients with asthma and/or rhinitis 1266-1272.
in China. Allergy 2009; 64: 1083-1092. [24] Pekkarinen PT, von Hertzen L, Laatikainen
[13] Schuetze G, Storm van’s Gravesande K, T, Makela MJ, Jousilahti P, Kosunen TU,
Sparhold S, Frischer T, Kuehr J. Comparison Pantelejev V, Vartiainen E, Haahtela T. A dis-
between serial skin-prick tests and specific parity in the association of asthma, rhinitis,
serum immunoglobulin E to mite allergens. and eczema with allergen-specific IgE between
Pediatr Allergy Immunol 1999; 10: 138-142. Finnish and Russian Karelia. Allergy 2007; 62:
[14] Huss-Marp J, Darsow U, Brockow K, Pfab F, 281-287.
Weichenmeier I, Schober W, Petersson CJ,
Borres MP, Ring J, Behrendt H. Can immuno-
globulin E-measurement replace challenge
tests in allergic rhinoconjunctivits to grass pol-
len? Clin Exp Allergy 2011; 41: 1116-1124.
2075 Int J Clin Exp Med 2016;9(2):2067-2075You can also read
