Original Article Atopic disease presentation in northeastern China: a 10-year retrospective study

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Original Article Atopic disease presentation in northeastern China: a 10-year retrospective study
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):2067-2075
Atopic 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

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Atopic 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-

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Atopic 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

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Atopic 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):2067-2075
Atopic 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):2067-2075
Atopic 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-
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