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Journal of Asthma
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/ijas20
Patterns of allergen sensitization in patients with
asthma in Yaqui Valley, Mexico
Diego Hazael Ramirez-Leyva, Leticia Díaz-Sánchez, Maria Citlaly-Ochoa &
Jose Manuel Ornelas-Aguirre
To cite this article: Diego Hazael Ramirez-Leyva, Leticia Díaz-Sánchez, Maria Citlaly-Ochoa &
Jose Manuel Ornelas-Aguirre (2021): Patterns of allergen sensitization in patients with asthma in
Yaqui Valley, Mexico, Journal of Asthma, DOI: 10.1080/02770903.2021.1941086
To link to this article: https://doi.org/10.1080/02770903.2021.1941086
Published online: 17 Aug 2021.
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JOURNAL OF ASTHMA
Patterns of allergen sensitization in patients with asthma in Yaqui Valley,
Mexico
Diego Hazael Ramirez-Leyva, MD, MEda, Leticia Díaz-Sánchez, MDb, Maria Citlaly-Ochoa, MDc and Jose
Manuel Ornelas-Aguirre, MD, MScd
aFamily Medicine, Instituto Mexicano del Seguro Social, Ciudad Obregón, México; bAllergology and Immunology, Instituto Mexicano
del Seguro Social, Ciudad Obregón, México; cPediatric Pneumology, Instituto Mexicano del Seguro Social, Ciudad Obregón, México;
dUniversidad de Sonora, Department of Health Sciences, Ciudad Obregón, México
ABSTRACT
Introduction:People who live in highly allergenic regions have a greater risk of being
sensitized; therefore, these areas have a higher prevalence of mono and polysensitized
patients. The aim of the present study was to investigate the allergen sensitization profiles
in patients with asthma in an agricultural zone in Mexico.
Methods:An analytical cross-sectional study was conducted in a secondary care hospital
in Obregon City, Mexico. The allergen sensitization pattern profiles were analyzed through
a skin prick test (SPT) in 294 patients. Data was collected before SPT: asthma control was
classified according to the Global Initiative for Asthma Criteria, nutritional status was assessed
with the Body Mass Index (BMI) using Quetelet’s index (BMI = weight/height2), and
comorbidities, asthma, and smoking habits were collected from the patients’ medical records.
Results:In this study, in a group of adults with asthma, the prevalence of sensitization was
77%. The most frequent categories of aeroallergens were in indoors, in zones with weeds
and abundant trees. A low proportion of monosensitized patients (2%) was observed. House
dust mites were the most common allergens.
Conclusions:Our study describes the sensitization pattern among asthma patients. This
study will help identify the panel of most common allergens in this region of Mexico, and
aid in selection of specific treatment through immunotherapy.
Introduction
Variat i o n in allergen sensitivity patterns is conditioned
by climate change, the degree of environmental pol-
lution, disruption in the microenvironments, and cul-
tural traits (1). These different patterns may explain
discrepancies in the prevalence of asthma, primarily
in patients with atopy (2). In Mexico, the prevalence
of asthma is 7%, ranging from 1.2% to 15% according
to geographical region (urban or agriculture zones,
with or without grass, and excess use of pesticides) (3).
Allergy diseases are highly prevalent chronic con-
ditions that can start from an early age and are medi-
ated by type 1 hypersensitivity reactions (4); and
respiratory allergies are the most frequent in this
group with a prevalence of 10 to 30% in adults world-
wide (5). A patient with an allergy produces immu-
noglobulin E (IgE) against a specific substance that
causes an exaggerated response in the immune system:
these substances are called allergens and are classified
into aeroallergens and food allergens (6).
Allergen exposure is clinically manifested as: rhi-
nitis, urticaria, dermatitis, conjunctivitis, gastrointes-
tinal symptoms, or asthma (7). The most important
diagnostic tool in the study of allergies is a thorough
medical history, and the identification of allergens
involved (8). Knowledge of the sensitization pattern
through the skin prick test (SPT) is a key element in
defining specific treatment lines (9); and treatment
alternatives are focus ed on administering an
allergen-specific immunotherapy that is used in desen-
sitization to allergens, suppression of allergic inflam-
mation, and for allergen-specific immune tolerance (10).
People who live in highly allergenic regions are at
greater risk of being sensitized; hence, these areas show
a higher prevalence of mono and polysensitized patients
(11). The Yaqui Valley, known as the granary of Mexico,
is located at the southern end of the state of Sonora
between the Gulf of California and the “Sierra Madre
Occidental” in Northwest Mexico; and is a land with
intense agricultural activity in the middle of desert
scrubs and estuarine ecosystems.
© 2021 Taylor & Francis Group, LLC
CONTACT Jose Manuel Ornelas-Aguirre manuel.ornelas@unison.mx Universidad de Sonora, Ciencias de la Salud, Avenida Bordo Nuevo S/N,
Antiguo Ejido Providencia, Ciudad Obregón, 85010 México.
https://doi.org/10.1080/02770903.2021.1941086
ARTICLE HISTORY
Received 21 Januar y 2021
Revised 29 April 2021
Accepted 4 June 2021
KEYWORDS
Allergenic; asthma; atopy;
immunotherapy; skin prick test
2 D. H. RAMIREZ-LEYVA ETAL.
The Yaqui Valley has a hot, dry climate with a
summer rainy season. The type of vegetation is dry
jungle and desert, and the State is considered one of
the most allergenic in the country due to the region’s
wheat monoculture, which is supported by the avail-
ability of water from the Yaqui River that feeds the
entire region. Another factor that contributes to clin-
ical conditions is the use of agrochemicals which are
very reactive and highly allergenic, along with the
increased use of fossil fuels and the generation of
dusts from agriculture practices. The Yaqui Valley is
considered the “cradle of the green revolution" of
agriculture in Mexico and is home to the Yaqui indig-
enous tribes (12). The patterns of sensitization fluc-
tuate among different areas and populations, and in
Mexico there is presently no epidemiological data
about the sensitization rate of common allergens in
the Yaqui Valley. Consequently, we aimed to investi-
gate the allergen sensitization profiles in patients with
asthma and the relationship of these profiles with
uncontrolled disease in an agricultural zone of Mexico.
Material and methods
Study design and population
An analytical cross-sectional study was conducted
from March 2017 to December 2018, at the Regional
General Hospital #1 in Obregon City, Mexico. Patients
diagnosed with asthma according to the Global
Initiative for Asthma (GINA) (13), who were over
16 years of age, with at least one positive SPT; resi-
dents of the Yaqui Valley, who signed the informed
consent letter, were included. Patients with immuno-
suppression, cancer, diabetes mellitus; rheumatoid
arthritis, systemic lupus erythematosus, pregnancy;
and intake of tricyclic antidepressants, were excluded.
Data collection was done before the SPT with a
standardized data collection form: asthma control was
classified according to GINA criteria in three different
groups: controlled, partially controlled, and uncon-
trolled; nutritional status was assessed with the Body
Mass Index (BMI = weight/height2); active and passive
smoking were evaluated by direct question; and the
comorbidities such as allergic rhinitis and atopic der-
matitis, type of treatment, and the time of evolution
with asthma, were collected from the medical records.
Skin prick test
The SPT was performed using a standardized technique
(14): before SPT each patient had at least one medical
evaluation in the Allergy Division, a clinical history,
and paraclinical studies including complete blood
count, nasal cytology, urinalysis; stool ova and parasites,
chest x-ray, and spirometry, were performed. The sen-
sitization pattern was implemented with a panel of 47
glycerinated allergens (ROCEL® allergens, México) in
a concentration of 1:20 weight-volume: the panel
included nine indoor allergens; pollens from six grasses,
15 weeds and nine trees; and seven fungal allergens.
All patients were instructed to interrupt (one week
prior) medications that may affect the results (antihis-
tamines, systemic steroids, and leukotriene receptor
antagonists). Dermographism was evaluated before the
SPT. The allergen panel was selected according to the
local characteristics and previous studies in Mexico.
Skin prick tests were performed by a trained nurse
under the supervision of a certified allergist and immu-
nologist. On the volar surface of the forearms, the
application sites of each extract were marked at a dis-
tance of 2 centimeters from one another. Subsequently,
using the Osterballe technique (15), antigen drops were
applied. The punctures were made perpendicular to the
skin with Prestige® brand lancets (Nipro, USA), using
one for each puncture without causing bleeding to avoid
combination of the different extracts. Finally, a puncture
was made in the positive control and another in the
negative: histamine (10 mg/mL) was used as a positive
control, and saline solution as negative control. The size
of the wheals was recorded at 15 min by an allergist,
and a positive test was defined as an induration of at
least 3 mm greater than the negative control.
Allergen panel
Indoor allergens: dermatophagoides farinae (D. fari-
nae), dermatophagoides pteronyssinus (D. pteronyssi-
nus), blomia tropicalis, cockroach mix (Periplaneta
Americana and Blattella Germanica), mosquito, animal
hair (dog and cat) and mix of feather.
Tre e p ol le n: acacia spp, shinus molle, prosopis spp,
olea europaea, populus spp, alnus spp, pinnus spp, frax-
inus spp and liquidambar styraciflua.
We ed p ol l en : artemisia ludoviciana, artemisia tri-
dentata, artemisia vulgaris salsola pestifer, amaranthus
palmeri, chenopodium album, ambrosia trifida, ambro-
sia elatior, helianthus spp, atriplex bracteosa, cosmos
spp, rumex crispus, franseria tenuifolia, medicago sativa
and plantago major.
Grass pollen: zea mays, phleum pratense, holcus
halepense, lollium perene, capriola dactylon and agros-
tis alba.
Fungal: fusarium oxysporum, monilia sitophila, pen-
icillium notatum, aspergillus fumigatus, candida albicans,
cephalosporium spp and helminthosporium sativum.
JOURNAL OF ASTHMA 3
Statistical analysis
Each allergen was measured to detect the prevalence
of sensitization. Quantitative variables were described
as median and interquartile range (IQR), and quali-
tative variables were expressed as frequency and per-
centage. The assumption of normality was made by
the Kolmogorov-Smirnov test. The Chi-squared test
was used to analyze differences in categorical vari-
ables, and the Odds ratio was used to calculate risk.
In the multivariate analysis, logistic regression was
used to identify the variables associated with uncon-
trolled asthma according to predictive models, and
assumptions of logistic regression were tested. The
variables with highest p values were eliminated in
each model, and logistic regression was carried out
again using the remaining variables; while this process
was repeated successively and completed when all the
variables in the final model were significant (p < 0.05).
For data analysis, the IBM SPSS program, version 20
(Armonk, NY, USA) was used.
Ethics
The study was approved by the Local Health Research
and Ethics Committee #2603 of the Instituto Mexicano
del Seguro Social (IMSS) in Obregon City, Mexico;
with registration number R-2016–2601-32. The
research was carried out in accordance with Bioethical
Principles, the General Health Law regarding health
research in Mexico, and the Declaration of Helsinki.
All patients signed a letter of written and informed
consent. Patients under 18 years of age signed the
written informed agreement along with their legal
guardians who also signed the informed consent.
Results
A total of 384 skin tests were performed on patients
with asthma from the Yaqui Valley, and 90 were neg-
ative for skin reaction (n = 294). Two hundred and
thirty-eight (81%) were female, and 56 (19%) were
male: the median age was 44 (21 IQR) years. The
most frequent atopic comorbidities were allergic rhi-
nitis (94%), and atopic dermatitis (13%). Asthma con-
trol based on the Global Initiative for Asthma (GINA)
was balanced: 110 (37%) controlled, 84 (29%) partially
controlled, and 100 (34%) uncontrolled.
Regarding nutritional status, the median BMI was
28.1 (IQR 7.8) kg/m2: 114 (38%) had obesity, 90 (31%)
were overweight (and this was identical for normal
weight); and there were no underweight patients
recorded. Active or passive smoking was found in 88
(30%) patients. The time since asthma diagnosis had a
median of 6 (IQR 13) years, and most patients (56%)
had had this disease for more than 6 years. Characteristics
of the patients are described in Ta b le 1 . The number
of positive skin tests had a median of 10 (IQR 5).
According to positive results, they were classified as
monosensitized (2%), and polysensitized (98%); and
most participants were sensitized to more than 10 aller-
gens (53%). The prevalence of main allergens by cate-
gory is described in Figure 1.
The most frequent indoor allergens were: D. ptero-
nyssinus 44%, D. farinae 43%, Blomia tropicalis 40%,
and cockroach mix 39%. In pollens, the most frequent
were: Amaranthus palmieri (weed) 37%, prosopis spp
(tree) 33%, ambrosia trifida (weed) 30%, European olea
(tree) 29%, salsola pestifer (weed) 27%, plantago major
(weed) 26%, and phleum pratense (grass) 25%. In fungi,
greater sensitization was found to Aspergillus fumigatus
27%, candida albicans 6%, and cephalosporium spp 2%.
Only five patients were monosensitized to mosquito
(n = 3) and cockroach mix (n = 2) (Ta bl e 2 ).
There were 110 (37%) patients with controlled
asthma, and 184 (63%) uncontrolled (including partially
controlled) asthma. Ta bl e 3 specifies the association
between the most common allergens and uncontrolled
asthma: Blomia tropicalis and D. pteronyssinus allergens
had the highest OR values. Tab l e 4 identifies the clin-
ical characteristics associated with uncontrolled asthma.
The multivariate analysis and the models are shown in
Ta bl e 5 , demonstrating that the variables with the high-
est association were obesity (OR = 4.0; 95% CI = 2.2
to 7.4), tree pollen (OR = 3.3; 95% CI = 2.0 to 5.6),
Blomia tropicalis (OR = 4.3; 95% CI = 2.4 to 7.7),
Table 1. Baseline characteristics of patients.
Characteristic (n = 294) n (%) 95% CI
Age – yr 44 (21)a–
Asthma evolution time – yr 6 (13)a–
Body Mass Index – kg/m228.1 (7.8)a–
Positive SPT 10 (5)a–
Sex
Male 56 (19) (9 to 29)
Female 238 (81) (76 to 86)
Nutritional status
Normal weight 90 (31) (21 to 41)
Overweight 90 (31) (21 to 41)
Obesity 114 (38) (29 to 47)
Asthma control
Controlled 110 (37) (28 to 46)
Partially controlled 84 (29) (19 to 39)
Uncontrolled 100 (34) (25 to 43)
Smoking 88 (30) (20 to 40)
Atopic comorbidity
Allergic rhinitis 276 (94) (91 to 97)
Atopic Dermatitis 38 (13) (2 to 24)
Monosensitization 5 (2) (−10 to 14)
yr = years, kg/m2 = Quetelet index, a = median (interquartile range), n =
frequency, % = percentage, SPT = skin prick test, 95% CI = 95%
Condence inter val.
4 D. H. RAMIREZ-LEYVA ETAL.
Atriplex bracteosa (OR = 4.4; 95% CI = 2.0 to 9.4)
and Olea europaea (OR = 3.1; 95% CI = 1.5 to 6.2).
The final model (Ta bl e 6 ), which is based on the
previously described covariates, identifies the main
factors associated with uncontrolled asthma.
Discussion
The most important finding in our study was the
high prevalence of aeroallergens in the Yaqui Valley.
These allergens could be strongly associated with the
development of asthma without being the sole or main
cause. A description of the most frequent allergens
was the main objective of this investigation, and, like
previous studies, the presence of obesity was found
to be an associated factor for uncontrolled asthma in
combination with some common allergens in the
Ya q u i Va l l e y ( 16). There were important differences
between groups according to disease control: patients
with uncontrolled asthma were older, had a higher
body mass index, a higher number of allergens in the
SPT, and a longer time since asthma diagnosis.
In order to develop, the allergy sensitization mech-
anism requires a combination of factors such as atopy,
abundant presence of allergens in the environment,
and continuous exposure time: some allergens can be
universal due to their characteristics, and others are
locally specific according to weather and vegetation.
The prevalence of sensitization to at least one allergen
in adults with asthma can be up to 82% (9), a result that
is similar to our study (77%) where the most frequent
categories of aeroallergens were indoors, weeds and trees,
which correlates with other studies in Western Mexico
(1), China (17), and the Middle East (18).
Asthma and allergic rhinitis
The global prevalence of allergic rhinitis in patients
with asthma is 80 to 90% (5), and the present study
had similar findings (93%). Some epidemiological and
pathophysiological studies suggest a close relationship
of this binomial distribution and have shown that
allergic rhinitis is a risk factor for asthma (19). The
prevalence of both diseases in the same person has
Figure 1. Frequency of allergen sensitization by category.
Table 2. Sensitization frequency to main allergens in the Yaqui
Valley.
Allergens (n = 294) n (%) 95% CI
Indoors
Dermatophagoides
pteronyssinus
130 (44) (35 to 53)
Dermatophagoides farinae 126 (43) (34 to 52)
Blomia tropicalis 116 (40) (31 to 49)
Cockroach mix 114 (39) (30 to 48)
Trees
Prosopis spp 96 (33) (23 to 42)
Europaean olea 86 (29) (19 to 39)
Alnus spp 58 (20) (10 to 30)
Weeds
Amaranthus palmeri 108 (37) (28 to 46)
Ambrosia trida 88 (30) (20 to 40)
Salsola pestifer 78 (27) (17 to 37)
Plantago major 76 (26) (16 to 36)
Artemisia vulgaris 68 (23) (13 to 33)
Grass
Phleum pratense 74 (25) (15 to 35)
Zea mayz 54 (18) (8 to 28)
Agrostis alba 44 (15) (4 to 26)
Fungal
Aspergillus fumigatus 78 (27) (17 to 37)
Candida albicans 18 (6) (−5 to 17)
Cephalosporium spp 6 (2) (−9 to 13)
n = frequency, % = percentage, 95% CI = 95% Condence interval.
JOURNAL OF ASTHMA 5
been verified in other studies (1,17,20) and is consis-
tent with our results.
An interesting outcome is the high proportion of
polysensitized patients (98%), while apparently the
main cause of acquiring multiple sensitivities is high
exposure to environmental allergens, for example by
occupational exposure or preexisting inflammatory
diseases; and sensitization to multiple allergens does
not alone explain the presence of asthma since there
are more determining risk factors such as genetics,
excessive dietary sugar consumption, indoor air qual-
ity, and pollution (21,22). This result is analogous
with previous studies done in Mexico (1), although
it differs from other studies in the Middle East
(18%), South America (36%), Canada (25%), and
Europe (17%).
Table 3. Prevalence of skin prick test reactivity to common allergens according to GINA.
Asthma control
Allergen
Uncontrolled*
n (%)
Controlled
n (%)
Odds ratio
(95% CI) p value
D. pteronyssinus 98 (53) 32 (29) 2.7 (1.6 to 4.5) <0.001
D. farinae 92 (50) 34 (31) 2.2 (1.3 to 3.6) <0.001
Blomia tropicalis 96 (52) 20 (18) 4.9 (2.7 to 8.6) <0.001
Cockroach mix 60 (33) 54 (49) 0.5 (0.3 to 0.8) 0.005
Amaranthus palmeri 78 (42) 30 (27) 1.9 (1.1 to 3.2) 0.009
Aspergillus fumigatus 38 (21) 40 (36) 0.45 (0.2 to 0.7) 0.003
Prosopis spp 70 (38) 26 (24) 1.9 (1.1 to 3.3) <0.001
* = uncontrolled and partially controlled, n = frequency, % = percentage, p = Chi-Squared test, 95% CI = 95% Condence interval, spp = species.
Table 4. Clinical characteristics associated with uncontrolled asthma.
Asthma control
Allergen
Uncontrolled*
(n = 184)
Controlled
(n = 110)
Odds ratio
(95% CI) p value
Agea46 (17) 40 (17) –<0.001c
BMIa30.3 (7.2) 25.1 (5.6) –<0.001c
Number of allergensa12 (6) 9 (6) –<0.001c
Time since diagnosisa8 (12) 5 (12) –0.002c
Sexb
Male 34 (19) 22 (20) 0.9 (0.4 to 1.6) 0.74d
Female 150 (81) 88 (80)
Obesityb96 (52) 18 (16) 5.5 (3.1 to 9.9) <0.001d
Allergic Rhinitisb172 (94) 104 (95) 0.8 (0.3 to 2.2) 0.71d
Atopic Dermatitisb12 (7) 26 (24) 0.2 (0.1 to 0.4) <0.001d
Smokingb62 (34) 26 (24) 1.6 (0.9 to 2.8) 0.06d
* = uncontrolled and partially controlled, a = median (interquartile range), b = frequency (percentage), c = Mann-Whitney U test, d = Chi-squared test,
BMI = body mass index, 95% CI = 95% Condence interval.
Table 5. Multivariate model of factors associated with uncontrolled asthma.
Multivariate analysis
Models β (SE) Wald OR (95% CI) p value
Clinical factors
Obesity 1.4 (0.31) 20.45 4.0 (2.2 to 7.4) <0.001
Age (<35 yr) −0.8 (0.30) 6.92 0.4 (0.2 to 0.8) 0.009
Evolution (1-5 yr) 0.6 (0.27) 4.73 0.5 (0.3 to 0.9) 0.03
Allergen categories
Tree pollen 1.2 (0.25) 22.70 3.3 (2.0 to 5.6) <0.001
Indoor allergens
D. pteronyssinus 0.8 (0.27) 8.95 2.2 (1.3 to 3.8) 0.003
Dog hair 1.1 (0.49) 4.90 3.0 (1.1 to 7.9) 0.02
Blomia tropicalis 1.4 (0.29) 24.57 4.3 (2.4 to 7.7) <0.001
Grass and weed pollen
Capriola dactylon 0.9 (0.49) 3.74 2.6 (0.9 to 6.9) 0.04
Atriplex bracteosa 1.4 (0.38) 14.73 4.4 (2.0 to 9.4) <0.001
Plantago major 1.2 (0.39) 10.18 3.5 (1.6 to 7.5) <0.001
Tree pollen
Prosopis spp 0.6 (0.28) 5.69 1.9 (1.1 to 3.4) <0.001
Alnus spp 1.0 (0.43) 5.74 2.8 (1.2 to 6.6) <0.001
Olea europaea 1.1 (0.34) 10.92 3.1 (1.5 to 6.2) <0.001
β (SE) = Beta coecient (standard error), OR = Odds ratio obtained through logistic regression, yr = years, 95% CI = 95% Condence interval, spp = species.
All covariates were introduced as categorical variables.
6 D. H. RAMIREZ-LEYVA ETAL.
Indoor allergens
Mexico has different climate conditions depending on
the zone. The Yaqui Valley (Sonora State) is charac-
terized as being dry and very hot, especially during
the summer, and this situation could explain the high
prevalence of indoor allergens, especially house dust
mites. Previous studies have shown great differences
in mite sensitization within Mexico, with the highest
rates in humid and semi-hot areas, and the lowest in
dry and temperate areas. In the Northwest, in a pre-
vious study, the prevalence was 53%, which was close
to our results (44%).
In Mexico, house dust mites are the most common
allergens present in patients with allergic diseases like
asthma (1,23,24). In countries like Iran and in the
Asia-Pacific region, these are the main sensitizers
(17,25) with higher frequencies than in Mexico.
Sensitization to indoor allergens has been described
as the main allergen category in asthma, causing bron-
chial hyperreactivity and uncontrolled disease (24),
which agrees with our findings.
The main house dust mites are D. pteronyssinus, D. fari-
nae and Blomia tropicalis, which have a close sensitization
frequency among them, and high levels of co-sensitizations
due to their homologous amino acid sequence and phylo-
genetic tree (26); and these allergens are the main sensitizer
worldwide in patients with atopy, regardless of age, country,
or weather (17,18,24,25). The D. pteronyssinus was the third
most important risk factor for uncontrolled asthma, and
patients sensitized to this allergen had four times more risk
of being uncontrolled (OR = 4.0; 95% CI = 2.0 to 8. 0).
Other interior allergens are dog and cat hair, for
which we found a low prevalence like previous studies
in Mexico (6 to 17%) and some regions of France
(4%) but differing from Middle East countries where
the prevalence is 36 to 78% to any animal hair;
whereas China reports 25% to dog hair, and Canada
53% sensitization to cat hair. In the Yaqui Valley,
cockroach mix was the fifth most frequent interior
allergen but the second excluding house dust mites,
whereas the frequency is higher in the Yaqui Valley
(40%) than other studies in Mexico (7%), China
(31%), France (2%), and the Middle East (32%). The
analysis between cockroach mix and uncontrolled
asthma showed a close association (OR = 0.5; 95%
CI = 0.3 to 0.8), but this result was not significant
in the multivariate model.
Pollens and asthma
Concentrations of airborne pollens in the State of
Sonora have an inter- and intra-annual variation. A
previous study shows that the annual total was 16,243
pollen day/m3 (2016), and 7899 pollen day/m3 (2018)
with two peaks: one from March-April, with concen-
trations around 500 pollen day/m3, and from
June-October, with higher concentrations ranging
from 800 to 2450 pollen day/m3 (27). Pollens are the
most frequent outdoor allergens worldwide (18), and
in Yaqui Valley this category placed second in fre-
quency. The pollens were divided into weed, tree and
grass: in the sub-category of weed, pollen of the ama-
ranthus palmeri was the most frequent; in trees, pro-
sopis spp; and in grass, phleum pratense, with close
frequencies between each one. In Guadalajara (Western
Mexico), the pollen category is the main sensitizer in
adults with allergic disease, and tree pollen is the
most frequent (Quercus spp); but in asthma patients,
house dust mites are the main sensitizer, followed by
cockroaches, and weed pollen (9), which is consistent
with our results.
In the Yaqui Valley, Mesquite (Prosopis spp) is dis-
tributed extensively; and so, it was the most frequent
tree pollen among asthma patients, but in the final
model this type of pollen was not associated with
uncontrolled asthma. Pollens that showed association
to asthma were: alnus spp (tree pollen) which gives
three times more risk for uncontrolled asthma; cap-
riola dactylon (grass pollen), conferring three times
more risk; and atriplex bracteosa (weed pollen), con-
ferring six times more risk. This result shows the
diversity of factors associated with uncontrolled
asthma in the final model (Ta ble 6 ); and in this
model, the risk factors were distributed as one clinical
factor, one indoor allergen, one tree pollen, one weed
pollen, and one grass pollen.
A study done in Western Mexico in children with
asthma showed a similar pattern in the frequency of
sensitization to pollen from weeds, grasses, and trees
(1). In weed pollen, Middle East countries report high
frequencies (64 to 77%) (28), which are similar to
our findings since these countries have comparable
Table 6. Final multivariate model of factors associated with
uncontrolled asthma.
Multivariate analysis
Final Model β (SE) Wald OR (95% CI) p value
Obesity 2.2 (0.37) 35.31 9.2 (4.4 to 19.1) 0.001
D. pteronyssinus 1.3 (0.34) 16.13 4.0 (2.0 to 8.0) 0.001
Capriola dactylon 1.3 (0.64) 4.13 3.7 (1.04 to 13.1) 0.04
Atriplex 1.9 (0.44) 18.54 6.7 (2.8 to 15.9) 0.001
Alnus spp 1.3 (0.49) 6.94 3.7 (1.3 to 9.8) 0.008
β (SE) = Beta coecient (standard error), OR = O dds ratio obtained through
logistic regression, 95% CI = 95% Condence interval, spp = species. All
covariates were introduced as categorical variables.
JOURNAL OF ASTHMA 7
climate conditions. In China, there is a higher fre-
quency of sensitization to Artemisia (13%) and
Ambrosia (12%), but at a lower percentage than our
study (30% and 23%, respectively). In Canada, the
most frequent pollen was grass pollen with 39%,
resembling Yaqui Valley findings.
Fungal sensitization
Fungal allergy is a common problem worldwide, and
sensitization to this allergen is a leading cause of
allergic diseases, uncontrolled asthma, and exacerba-
tion of respiratory symptoms (29). In Mexico, some
studies found that the most frequent fungi are
Aspergillus fumigatus, candida albicans, and alternalia
alternata (20), in that order. Although the present
study did not include alternaria alternata, the same
pattern of prevalence in Aspergillus fumigatus and
candida was found. The prevalence of Aspergillus
fumigatus was similar to previous studies in Sonora
(22%) and Michoacán (23%), but higher than Jalisco
(3%), Nuevo Leon (3%), and Mexico City (17%).
There are important differences in the prevalence
of Aspergillus fumigatus sensitization worldwide:
Europe shows a variation from 0.4% (Italy) to 10.3%
(Greece), in the United States 10%, Africa 52%, and
Central America 16%, which is lower than our results.
Countries in the Middle East with high humidity and
temperature have a prevalence of 25% (28), like the
Ya q u i Va l l e y d u e t o w e a t he r c o n d i t i on s . Aspergillus
fumigatus is the fungus that most sensitizes patients
with allergic diseases, especially asthma (30).
In Candida genus, our findings are lower than other
cities in Mexico such as Michoacán (19%), Jalisco
(17%), and Mexico City (16%); while in Middle East
cities the prevalence is high in asthma patients (53%).
Candida is a genus of yeasts with many species that
are common to the skin and the gastrointestinal and
genitourinary tracts. Candida is the most frequently
isolated species and many studies have suggested that
it plays an important role in allergy diseases (31).
Exposure to fungi is mainly in outdoor environ-
ments but it can be an indoor allergen in the right
conditions and can even grow on interior surfaces and
materials. A previous study on fungal airborne con-
centration in the Yaqui Valley shows that the annual
total was 1,690 spores day/m3 and the peaks were
recorded in March, July, August, and December, reach-
ing monthly indices of up to 200 spores (32). The high
humidity and temperature allow the growth and devel-
opment of fungi in the Yaqui Valley. In this region of
Mexico, the annual relative humidity is, on average,
45%, with a rainfall of about 450 mm annually, which
theoretically supports the fungus proliferation in this
environment. Although temperature and humidity are
adequate, the category with the lowest prevalence of
sensitization was fungi, which could be explained by
the geographical location, since being a valley near the
coast supports the dispersal of fungi by the wind. On
the other hand, pollen from weeds, trees, and grasses
predominated in the category of outdoor allergens, in
that order, which is consistent with the local ecosystem.
There is a relationship between fungal sensitization
and the severity of allergic diseases (31), and in our
investigation the severity of asthma was not considered,
but in the final model this category was not relevant.
The presence of fungi in outdoor and indoor environ-
ments is not equivalent to sensitization but given the
correct conditions fungi play an important role in trig-
gering respiratory symptoms in patients with asthma.
Obesity and asthma
Asthma control was found to be balanced according
to the Global Initiative for Asthma categories. The
final dichotomy showed 66% of patients with uncon-
trolled asthma (uncontrolled and partially controlled).
This uncontrolled asthma may be an incidental find-
ing related to the recruitment location, since our hos-
pital is a regional referral center with specialization
in allergology, and patients are sent by their initial
treating physician in the case of recurrent or poor
response to treatment; therefore, an elevated number
of patients with uncontrolled asthma is to be expected.
Obesity is a risk factor for the development of asthma
and impaired mechanical function of the chest, and
it influences treatment response and severity of symp-
toms (33). The role of obesity in severe asthma shows
characteristics related to BMI, supporting the theory
that severe asthma associated with obesity may rep-
resent a new clinical phenotype.
Obesity is associated with poor control and with
severity of respiratory symptoms, a result that is con-
sistent with our population, as we found a nine-fold
increased risk for uncontrolled asthma in people with
obesity, and it is the main risk factor for uncontrolled
asthma in our population. Interventions that promote
lifestyle modifications and weight loss represent an
important area of opportunity that will contribute to
symptom and overall clinical improvements.
Strengths and weaknesses
The main strength of the present study is being the
first carried-out directly in the Yaqui Valley, and
8 D. H. RAMIREZ-LEYVA ETAL.
although there are previous studies done in Northwest
Mexico, they do not show data from this important
area. Another advantage is in the recruitment of
patients during all seasons, which reduces the selec-
tion bias secondary to seasonal variation of allergic
diseases. With regards to weaknesses, the data about
sensitization are only regional, but it could still be
useful for people living in other countries. The inves-
tigation was conducted in patients with allergic dis-
eases and not in the general population, we didn’t
follow the population over time, and did not control
for variables such as air pollution (pesticides, for
example), the presence of mold at home, and the
diet. Despite these limitations our results are useful
for patients with asthma and allergic rhinitis. The
profile of sensitization was made through SPT, and
quantitative measurement of the size of wheals, or
IgE concentration, could contribute with more infor-
mation on the allergy profile. Many studies describe
the severity of asthma symptoms and their associa-
tion with allergens, but we focused on disease con-
trol, and for this reason comparison with other
studies was limited.
Conclusion
In conclusion, we found that indoor allergens (espe-
cially house dust mites) and weed pollen were the most
frequent allergens in the Yaqui Valley. Our study
describes the sensitization pattern among asthma
patients, which is an important tool for diagnosis and
treatment of allergic diseases. Obesity was found to be
another factor associated with asthma. This can be
explained by an inflammatory response through diet;
with actions directed at encouraging an anti-inflammatory
diet as a fundamental part of the treatment. Sensitization
to allergens is not enough to diagnose allergic diseases,
and the presence of specific symptoms is necessary for
finding the source through SPT or specific IgE. This
study will help identify the panel of most common
allergens in the Yaqui Valley for performing skin prick
tests and for identifying specific treatment through
immunotherapy.
Acknowledgements
The authors wish to thank the Instituto Mexicano del Seguro
Social for their support in this project, the authorities of
the Regional General Hospital #1 in Obregon City, and the
staff of the Allergy Division for their commitment and
professionalism. Special thanks to Alan Urbina-Alvarez for
the Spanish to English translation.
Author contributions
RLDH and DSL designed the study. RLDH wrote the man-
uscript. OMC contributed to data collection. RLDH and
JMOA performed the statistical analysis and interpretation of
the results. All authors read and approved the nal manuscript.
Declaration of interest
e authors report no conicts of interest.
ORCID
Jose Manuel Ornelas-Aguirre http://orcid.org/0000-0002-
6225-7587
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