595779

research-article2015
IJI0010.1177/0394632015595779International Journal of Immunopathology and PharmacologySpinozzi et al.

Letter to the editor

International Journal of

Characteristics and predictors of allergic Immunopathology and Pharmacology

2016, Vol. 29(1) 129­–136
© The Author(s) 2015
rhinitis undertreatment in primary care Reprints and permissions:
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DOI: 10.1177/0394632015595779
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F Spinozzi,1 N Murgia,2 S Baldacci,3 S Maio,3 AP Pala,4

C Casciari,1 M dell’Omo,2 and G Viegi,3,5 on behalf of ARGA study group

Abstract
Although allergic rhinitis is considered a raising medical problem in many countries it is often undertreated. The reasons
for this phenomenon are not completely clear.
The aim of this study is to evaluate factors associated with allergic rhinitis under-/no treatment.
A sample of 518 allergic rhinitis patients recruited by their primary care physicians, as a part of the ARGA study, were
invited to fill in a specific questionnaire regarding rhinitis symptoms, treatment, and rhinitis-related work/social disability.
Chi-square test and logistic regression were performed to assess risk factors for allergic rhinitis under-/no treatment.
Over one out of four patients had no treatment despite the symptoms and 13.5% were inadequately treated.
Participants with asthma (OR 0.47, 95% CI 0.30–0.75) and conjunctivitis (0.44, 95% CI 0.27–0.71) were at lower risk
of allergic rhinitis under-/no treatment: in asthmatics this reduction was related mainly to the concomitant asthma
treatment (OR 0.19, 95% CI 0.10–0.37).
Asthmatics with under-/not treated rhinitis had the highest prevalence of rhinitis-related quality of life impairment.
Under-/no treatment for allergic rhinitis is still rather frequent despite the relevance of this disease. The simultaneous
presence of asthma and an anti-asthmatic therapy are able to influence positively the treatment. Targeted interventions
toward a better characterization and a tight follow-up of rhinitis patient without asthma are needed.

Keywords
allergic rhinitis, asthma, conjunctivitis, general practitioners, medicines, perennial, quality of life, seasonal, treatment,
undertreatment

Date received: 6 October 2014; accepted: 17 June 2015

Introduction
Allergic rhinitis is characterized by a considerable 1Laboratory of Experimental Immunology and Allergy, Department
medical and social burden, mainly because of its of Medicine, University of Perugia, Piazzale Gambuli, 06100 Perugia,
high prevalence in industrialized countries, the Italy
2Section of Occupational Medicine, Respiratory Diseases and
relationship with asthma and the impact on quality Toxicology, University of Perugia, Piazzale Gambuli, 06100 Perugia,
of life.1,2 In Italy, a rise in allergic rhinitis preva- Italy
lence, from 16.8% to 25.8% over the last 20 years, 3Pulmonary Environmental Epidemiology Unit, CNR Institute of Clinical

Physiology, Via Trieste 41, 56126 Pisa, Italy

in a particular setting has recently been reported.3 4Technosciences Unit, CNR Institute of Clinical Physiology, Via Trieste
Furthermore, there is increasing evidence that 41, 56126 Pisa, Italy
allergic rhinitis is also a rising medical issue in 5CNR Institute of Biomedicine and Molecular Immunology “A.

regions of the world other than Europe and North Monroy”, Via Ugo La Malfa 153, 90146 Palermo, Italy

America.4 Besides, the economic impact of allergic Corresponding author:

rhinitis remains substantial: in the USA, the total Nicola Murgia, Section of Occupational Medicine, Respiratory Diseases
and Toxicology, University of Perugia, Piazzale Gambuli, 06100 Perugia,
direct medical cost of allergic rhinitis is approxi- Italy.
mately $3.4 billion per year;5 in Sweden the cost of Email: [email protected]
130 International Journal of Immunopathology and Pharmacology 29(1)

rhinitis in terms of lost productivity is €2.7 billion allergic rhinitis by ARIA guidelines;13 among
per year.6 Such data reinforce the need to imple- them, 144 were excluded due to missing informa-
ment the guidelines for early diagnosis and effec- tion (e.g. sex, age, answers to the key questions).
tive treatment of allergic rhinitis prepared by Each of the 518 participants provided written
scientific societies and expert panels.7 However, informed consent for the participation in the study,
allergic rhinitis is still considered a trivial disease anonymous management of individual and collec-
by some physicians, resulting often in underdiag- tive data, as well as anonymous publication of the
nosis and inadequate treatment.8 Recently, some research results. The study protocol, patient infor-
authors also pointed out that patients’ compliance mation sheet, and consent form were approved by
to the treatment, properly prescribed by their phy- the Ethic Committee of the Region Umbria (CEAS
sicians, is very poor.9 Under-/no treatment of aller- Umbria).
gic rhinitis is associated with delayed medical
examinations, patient preference for non-prescrib- Questionnaire
ing drugs, and the fear of drug-related costs, but
the specific characteristics of patients undertreated “Allergic rhinitis” was defined as having watery
or not treated for allergic rhinitis are still not com- runny nose with one or more of the following: (1)
pletely clear.7 Having information on which group nasal itching; (2) sneezing; and/or (3) nasal obstruc-
of patients needs more attention in terms of educa- tion.13 Symptoms were classified as perennial if
tion, follow-up, and adherence to the therapy could they were present almost all year round or seasonal
help tailoring practical interventions by general if they were present in just some seasons. Patients
practitioners and specialists toward a better control reporting a skin prick test (SPT) positive reaction
of allergic rhinitis symptoms. The aim of this study only to grass pollen and/or tree pollen and/or other
is to elucidate predictors of allergic rhinitis under-/ seasonal allergens were included in the category
no treatment in participants recruited by their gen- “seasonal allergens sensitization”, while a SPT
eral practitioners, as a part of the ARGA study,10–12 positive reaction only to dust mites and/or cat and/
focusing mainly on patients characteristics, type of or dog and/or other perennial allergens was defined
symptoms, and on the relationship between aller- as “perennial allergens sensitization”. If the patient
gic rhinitis and asthma. reported a SPT positive reaction to seasonal and
perennial allergens he/she was classified having
“both sensitization”. A SPT positive response to
Methods food was defined as “food allergens sensitization”.
Rhinitis-related quality of life (QoL) impairment,
Study population indicating a “disabling rhinitis”, was identified by
This survey is a part of the ARGA study an affirmative answer to one or more questions on
(‘Allergopatie Respiratorie: studio di monitoraggio sleep, work, and school or everyday life impair-
delle linee guida GINA e ARIA’),10 funded by the ment (Figure 2). Participants were classified as
Italian Drug Agency (AIFA) and performed having “asthma” if they reported in the question-
between March 2007 and February 2010. The naire asthma-like symptoms (wheezing, shortness
study was carried out in collaboration with a ran- of breath, chest tightness) or use of medication for
dom sample of 27 general practitioners (GPs) and asthma. To avoid a possible overlap with chronic
family pediatricians (FPs) of Perugia Province bronchitis and to increase the likelihood of asthma
(Umbria, Italy), an area of 671,820 inhabitants. diagnosis, a score system for some key questions
GPs and FPs were invited to administer a question- (e.g. having cough and phlegm as cough character-
naire to their patients when they came to their istic) was set up. Participants with allergic rhinitis
offices with symptoms suggesting an allergic rhini- who reported no treatment for this disease were
tis, enrolled consecutively, during the period classified as “not treated”, whereas participants
January 2008 to December 2009. All 750 patients with a rhinitis-related QoL impairment, character-
recruited by GPs and FPs were accepted to partici- ized by a poor control, who were treated just with
pate in the study; in Figure 1 the patient recruit- antihistamine and/or vasocostrictor as needed,
ment and selection flow chart are described. but needing by ARIA guidelines a more continu-
Briefly, 662 patients had symptoms suggesting ous treatment, were classified as “undertreated”.
Spinozzi et al. 131

Participants
n = 750

83 excluded because information on allergic rhinitis

were missing

5 subjects had no allergic

rhinitis

Subjects with allergic rhinitis

(AR)
n = 662

52 excluded because basic information (sex, age,

etc.) were missing

92 excluded because of incomplete answers to the

key questions

Subjects with AR forming the study population

n = 518

Subjects treated for Subjects not adequately treated for AR Subjects not treated
AR for AR
n = 70
n = 312 n = 136

Figure 1.  Flow chart of the study population enrolment and selection.

Patients not treated or undertreated formed the test. In one regression model the overall under-/no
category “under-/not treated” and in the logistic treatment risk was considered. Since the presence of
regression analysis (see below) were those having asthma appears an important factor also able to
“under-/no treatment”. influence rhinitis treatment, another regression anal-
ysis was performed in asthmatics only, adding a
Statistical analyses treatment for asthma as a possible influencing fac-
tor. The goodness of fit of the logistic regression
To assess the distribution of subject characteristics models was confirmed by the Hosmer-Lemeshow
among patients treated, not adequately treated and test.14 Statistical analyses were performed with the
not treated, the chi-square test was used; a two-tailed statistical software package SPSS Statistics 20.0
test with a 5% level of significance was considered (IBM SPSS, Chicago, IL, USA).
appropriate for the analysis. A similar subgroup
analysis was conducted dividing each treatment
class in subject with or without asthma, calculating
Results
chi-square test for trend. Risk factors for under-/no A total of 136 (26.3%) participants with self-
treatment were evaluated by logistic regression reported symptoms of allergic rhinitis received no
models, adjusting for sex and age. Independent vari- pharmacological treatment, 70 (13.5%) patients
ables were those factors not equally distributed in were undertreated; for reasons of sampling size
the different treatment categories by the chi-square comparability they were placed together in the
132 International Journal of Immunopathology and Pharmacology 29(1)

80
p<0.001
Treated without asthma
70
Treated with asthma
Undertreated/not treated without asthma
60 p<0.001
Undertreated/not treated with asthma

p<0.001
50

p<0.001
40
%

30

20

10

0
Rhinitis related quality Rhinitis related sleep Rhinitis related Rhinitis related daily
of life impairment impairment work/school impairment activities impairment

Figure 2.  Quality of life impairment of the allergic rhinitis patients treated and under-/not treated, divided by the occurrence of
asthma.

category “Under-/no treatment” and compared to In the logistic regression model performed in the
those treated (Table 1). whole population, adjusting for sex and age, par-
Almost all the patients (99.6%) had undergone ticipants with conjunctivitis or asthma had a lower
skin prick test for common aero-allergens which had risk of under-/no treatment (Table 3). In another
resulted positive (Table 1). The percentage of model, limited to asthmatics, the role of conjuncti-
patients with perennial symptoms and perennial vitis was confirmed and participants in treatment
allergens sensitization was higher in those under-/ for asthma were at lower risk of rhinitis under-/no
not treated, while the proportion of participants with treatment, whereas patients with perennial sensiti-
seasonal allergens sensitization was lower in this zation alone were at higher risk of rhinitis under-/
latter group (Table 1). Out of 518 patients, more no treatment (Table 4).
than an half (51.4%) reported a disabling rhinitis
causing a sleep/work/life impairment. After stratify- Discussion
ing the two categories of rhinitis patients by pres-
ence/absence of asthma (Table 2), those with asthma Main findings
showed higher frequency of perennial symptoms, as In this study risk factors for allergic rhinitis under-/
well as lower frequency of conjunctivitis. no treatment have been evaluated. The presence of
Prevalence of quality of life impairment signifi- asthma and conjunctivitis was associated with a
cantly increased from the group of patients treated more adequate treatment.
without asthma to the group of patients under- Allergic rhinitis undertreatment has previously
treated/not treated with asthma (Figure 1). This been explored but did not focus on individual/
trend was also evident for each of the three specific disease characteristics. For example, in a large
domains. European survey over half of patients with rhinitis
Spinozzi et al. 133

Table 1.  Characteristics of the allergic rhinitis patients treated and under-/not treated.

Partipants with AR treated Participants with AR under-/ P

(n = 312) not treated (n = 206)
Women (%) 52.2 55.8 NS
Age >15 years (%) 87.8 83.5 NS
Nasal obstruction (%) 96.8 96.1 NS
Nasal itching (%) 89.1 88.8 NS
Sneezing (%) 98.1 94.7 NS
Seasonal allergic rhinitis (%) 71.2 62.1 <0.05
Perennial allergic rhinitis (%) 28.8 37.9  
Nasal symptoms lasting 12 months (%) 97.4 94.2 NS
SPT performed (%) 99.4 100 NS
Atopy by SPT (%) 100 100 NS
Seasonal allergens sensitization (%) 40.2 29.6 <0.005
Perennial allergens sensitization (%) 10.9 22.3  
Both sensitization (%) 48.9 48.1  
Food sensitization (%) 7.1 3.9 NS
Rhinitis-related QoL impairment (%) 39.1 69.9 <0.01
Rhinitis-related sleep impairment (%) 28.5 52.4 <0.01
Rhinitis-related work/school impairment (%) 19.6 33.5 <0.01
Rhinitis-related daily activities impairment (%) 29.8 45.6 <0.01
Conjunctivitis (%) 65.7 53.4 <0.01
Asthma (%) 63.1 36.9 <0.01
Childhood onset asthma (%) 29.5 25.2 NS

AR, allergic rhinitis; SPT, skin prick tests.

Table 2.  Characteristics of the allergic rhinitis patients treated and under-/not treated divided by the occurrence of asthma.

Participants treated for allergic Participants with allergic rhinitis P

rhinitis under-/not treated

  Without asthma With asthma Without asthma With asthma

(n = 148) (n = 164) (n = 110) (n = 96)
Women (%) 51.4 53 57.3 54.2 NS
Age >15 years (%) 85.8 89.6 80.9 86.5 NS
Nasal obstruction (%) 98 95.7 99.1 92.7 NS
Nasal itching (%) 93.2 85.4 90.9 86.5 NS
Sneezing (%) 97.3 98.8 96.4 92.7 NS
Seasonal allergic rhinitis (%) 77.7 65.2 73.6 49 <0.001
Perennial allergic rhinitis (%) 22.3 34.8 26.4 51.0
Nasal symptoms lasting 12 months (%) 97.3 97.6 97.3 90.6 <0.05
Atopy by SPT (%) 99.3 100 100 100 NS
Seasonal allergens sensitization (%) 51 30.5 38.2 19.8  
Perennial allergens sensitization (%) 11.6 10.4 20.9 24 <0.001
Both sensitization (%) 37.4 59.1 40.9 56.2  
Food sensitization (%) 5.4 8.5 2.7 5.2 NS
Conjunctivitis (%) 95.5 59.8 84.9 38.5 <0.001

SPT, skin prick tests.

had not seen a physician in the last year, preferring of patients are still considering it as a trivial dis-
either non-prescription medication or nothing, ease.8 In our survey, over half of the patients had an
mainly due to the high cost of drugs.7 Hence, even impairment of their daily/social life, in particular
if allergic rhinitis is widely accepted as clinically sleep impairment, confirming previous findings.5
relevant and disabling,15 a not negligible proportion As regards sleep disturbances, it is to point out that
134 International Journal of Immunopathology and Pharmacology 29(1)

Table 3.  Predictors of allergic rhinitis under-/no treatment, serious symptoms throughout the year, not driving
adjusted for sex and age. them to seek for medical attention, or their doctors
ORa 95% CI P tend to concentrate their effort in treating the con-
Type of rhinitis
comitant asthma symptoms. Furthermore, partici-
Seasonal allergic rhinitis 1   pants with a perennial allergen sensitization, since
Perennial allergic rhinitis 1.35 0.85–2.15 NS symptoms usually are continuous, could underes-
Type of sensitization timate the importance of following a correct treat-
Seasonal allergens 1   ment. It is known that lack of efficacy, side effects,
Perennial allergens 1.96 1–3.86 NS treatment duration, and costs are associated with a
Both 1.23 0.77–1.95 NS lower compliance to allergic rhinitis treatment.18
Conjunctivitis
In a recent Spanish survey, just 15% of allergic
No  
Yes 0.44 0.27–0.71 <0.005
rhinitis patients sensitized to dust mites reported
Asthma an improvement after pharmacological treat-
No   ment.19 Another possibility would be that patients
Yes 0.47 0.30–0.75 <0.005 with perennial allergic rhinitis do not take ade-
quate treatment due to an effective allergen avoid-
ance. A recent update of the Cochrane Review on
Table 4.  Predictors of allergic rhinitis under-/no treatment in house dust mites avoidance and allergic rhinitis
asthmatics, adjusted for sex and age.
stated that dust mites impermeable bedding and
ORa 95% CI P other preventive measures are not proven to give a
Type of rhinitis substantial benefit to control rhinitis symptoms.20
Seasonal allergic rhinitis 1   The role of asthma in the difference between
Perennial allergic rhinitis 1.47 0.80–2.70 NS perennial and seasonal allergic rhinitis needs to be
Type of sensitization further evaluated. We have shown in another study,
Seasonal allergens sensitization 1   with general practitioners from other Italian
Perennial allergens sensitization 3.59 1.33–9.72 <0.05 regions, that GPs tend to be more compliant with
Both 1.69 0.82–3.51 NS
ARIA guidelines while treating allergic rhinitis
Conjunctivitis
No 1  
alone than allergic rhinitis  + asthma patients21.
Yes 0.44 0.25–0.79 <0.01 Conversely, in the present study in the Umbria
In treatment for asthma region, the logistic regression analysis, adjusting
No 1   for sex, age, and rhinitis symptoms/sensitization
Yes 0.19 0.10–0.37 <0.0001 seasonality, demonstrated that asthma and con-
junctivitis are the only two independent factors
able to influence the treatment for allergic rhinitis.
they might have an important effect on mental The results on asthma and conjunctivitis suggest
health, including increased depression, anxiety, and that those with associated co-morbidity might have
alcohol abuse.2 a more severe disease or be more aware of it; alter-
In the univariate analysis the prevalence of rhi- natively, they might just be more under control by
nitis under-/no treated was lower in patients with a their physician because of the associated diseases.
sensitization to seasonal allergens, the reason of When limiting the analysis to asthmatics patients,
this finding is to be elucidated. It is possible that this hypothesis is insofar as asthmatics under ther-
patients with seasonal sensitization and symptoms apy are at lower risk of rhinitis under-/no treat-
experience intense symptoms related to the peaks ment. It is known that in asthmatics a coexistent
of pollen exposure16 which drive them to seek for allergic rhinitis increases the severity of asthma11
medical attention. Indeed, global climate changes as well as the annual number of GPs visits,22 thus
have been related to increase in pollen concentra- increasing the likelihood to be properly treated also
tion over the last 20 years.17 On the other hand, in for allergic rhinitis. Moreover, the presence of ocu-
the univariate analysis participants with perennial lar symptoms worsens the quality of life of rhinitic
sensitization and symptoms tend to be under/not patients23 and this could push the patient to be more
treated, especially when asthma coexists. We compliant with the allergic rhinitis treatment since
hypothesize that either patients experienced less the pharmacological treatments are often the
Spinozzi et al. 135

same.13 As a matter of fact, the presence of con- treatment. Annals of Allergy Asthma & Immunology
junctivitis has been associated with an increased 106 Suppl 2: S12–16.
number of allergic rhinitis drug prescriptions.24 6. Hellgren J, Cervin A, Nordling S, et al. (2010)
A possible limitation of our study might be the Allergic rhinitis and the common cold–high cost to
society. Allergy 65: 776–783.
sample size. However, the peculiarity of the study
7. Maurer M and Zuberbier T (2007) Undertreatment of
population (a homogeneous group of participants
rhinitis symptoms in Europe: Findings from a cross-
coming from the same small Region, sharing the sectional questionnaire survey. Allergy 62: 1057–
same healthcare system, recruited by a small team 1063.
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analogous numbers in similar surveys25 may over- and rate of diagnosis of allergic rhinitis in Europe.
come such limitations. European Respiratory Journal 24: 758–764.
9. Loh CY, Chao SS, Chan YH, et al. (2004) A clini-
cal survey on compliance in the treatment of rhinitis
Conclusions
using nasal steroids. Allergy 59: 1168–1172.
In this study of patients with allergic rhinitis 10. Baldacci S, Maio S, Simoni M, et al. (2012) The
recruited by their primary care physicians, more ARGA study with general practitioners: Impact of
than 25% had no treatment despite the symptoms medical education on asthma/rhinitis management.
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of being under-/not treated. These findings
tioners. Journal of Asthma 49: 854–861.
strengthen the need of targeted educational inter- 12. Braido F, Comaschi M, Valle I, et al. (2012) Knowledge
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Declaration of conflicting interests Allergic rhinitis and its impact on asthma (ARIA)
The author(s) declared no potential conflicts of interest 2008 update (in collaboration with the World Health
with respect to the research, authorship, and/or publication Organization, GA(2)LEN and AllerGen). Allergy 63
of this article. Suppl 86: 8–160.
14. Hosmer DW and Lemeshow S (1989) Applied Logistic
Funding Regression. New York, NY: John Wiley & Sons.
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This study was a part of the ARGA study (‘Allergopatie Allergic rhinitis. Lancet 378: 2112–2122.
Respiratorie: studio di monitoraggio delle linee guida GINA 16. Annesi-Maesano I, Rouve S, Desqueyroux H, et al.
e ARIA’) supported by the Italian Drug Agency (AIFA). (2012) Grass pollen counts, air pollution levels and
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