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Gastritis and Gastroesophageal Reflux Disease Are Strongly Associated Finocchio et al. BMC Pulm Med (2021) 21:53 https://doi.org/10.1186/s12890-020-01364-8 RESEARCH ARTICLE Open Access Gastritis and gastroesophageal refux disease are strongly associated with non-allergic nasal disorders Eliana Finocchio1, Francesca Locatelli1, Francesca Sanna1, Roberta Vesentini1, Pierpaolo Marchetti1, Gianluca Spiteri2, Leonardo Antonicelli3, Salvatore Battaglia4, Roberto Bono5, Angelo Guido Corsico6, Marcello Ferrari7, Nicola Murgia8, Pietro Pirina9, Mario Olivieri2 and Giuseppe Verlato1* Abstract Background: Gastroesophageal refux disease (GERD) has been reported to be signifcantly associated with chronic rhinosinusitis, but the strength of the association is still debated. Aims: To evaluate the strength of the association between gastritis/GERD and non-allergic rhinitis (NAR)/allergic rhinitis (AR)/sinusitis. Methods: We investigated 2887 subjects aged 20–84 years, who underwent a clinical visit in seven Italian centres (Ancona, Palermo, Pavia, Terni, Sassari, Torino, Verona) within the study on Gene Environment Interactions in Respira- tory Diseases, a population-based multicase-control study between 2008 and 2014. Subjects were asked if they had doctor-diagnosed “gastritis or stomach ulcer (confrmed by gastroscopy)” or “gastroesophageal refux disease, hiatal hernia or esophagitis”. The association between NAR/AR/sinusitis and either gastritis or GERD was evaluated through relative risk ratios (RRR) by multinomial logistic regression. Results: The prevalence of gastritis/GERD increased from subjects without nasal disturbances (22.8% 323/1414) to subjects with AR (25.8% 152/590) and further to subjects with NAR (36.7% 69/188) or sinusitis (39.9%= 276/691). When adjusting for centre,= sex, age, education level, BMI, smoking habits and= alcohol intake, the combination= of gastritis and GERD was associated with a four-fold increase in the risk of NAR (RRR 3.80, 95% CI 2.56–5.62) and sinusitis (RRR 3.70, 2.62–5.23) with respect to controls, and with a much smaller increase= in the risk of AR (RRR 1.79, 1.37–2.35).. = = Conclusion: The study confrmed the association between gastritis/GERD and nasal disturbances, which is stronger for NAR and sinusitis than for AR. Keywords: Gastritits, Gastroesophageal refux disease, Allergic rhinitis, Non-allergic rhinitis, Sinusitis Background Rhinitis is a global common problem and is defned as the presence of at least one of the following: congestion, rhi- norrhea, sneezing, nasal itching, and nasal obstruction. *Correspondence: [email protected] Te two major classifcations are allergic (AR) and non- 1 Section of Epidemiology and Medical Statistics, Department of Diagnostic and Public Health, University of Verona, Strada Le Grazie, 8, allergic rhinitis (NAR) [1]. NAR occurs when obstruction 37134 Verona, Italy and rhinorrhea are related to non-allergic, non-infec- Full list of author information is available at the end of the article tious triggers such as a change in the weather, exposure © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Finocchio et al. BMC Pulm Med (2021) 21:53 Page 2 of 9 to caustic odors or cigarette smoke, barometric pressure as several studies which found an association between diferences, etc. [2]. Te prevalence of AR in adults in GERD and nasal disorders did not distinguish between Europe ranged from 17 to 28.5% [3], while NAR afects NAR and AR [22]. up to 30% of individuals in the Western population [4]. Since nasal disorders are highly prevalent diseases that Gastro-esophageal refux disease (GERD) is also a can have a deep impact on individual life and healthcare worldwide prevalent condition, which is on the rise in system, it is important to identify causative and trigger- Europe and North America [5]. Hence also esophageal ing factors, and their comorbidities. Te present study and extraesophageal diseases associated with GERD are aimed to investigate the relation between gastritis/GERD expected to increase. Some of the well-established extrae- and allergic and non-allergic rhinitis in a large popula- sophageal manifestations are refux-induced cough, lar- tion-based case–control study. yngitis, asthma and dental erosion. Other manifestations, such as sinusitis, pharyngitis, idiopathic pulmonary Methods fbrosis, and recurrent otitis media, are proposed but not Study design established as it is unclear whether GERD is a signifcant causal or exacerbating factor [6]. Te study was performed in the frame of the GEIRD Since both chronic rhinosinusitis and GERD are highly (Gene-Environment Interactions in Respiratory Dis- prevalent, it is difcult to establish a direct relation eases) study, a multicase-control study on respiratory between them, as they can easily coexist independently health, involving seven Italian centers, three located in [7]. Moreover, while the association between GERD and Northern Italy (Verona, Pavia, Turin), two in Central Italy nasal disorders gained support in children [8, 9], in adults (Ancona, Terni) and two in the major islands (Sassari in the evidence is still sparse. Several studies focused on Sardinia and Palermo in Sicily) [23]. Te study comprised the possible correlation of GERD and sinusitis [10–12], a screening phase and a clinical phase. In the screening which have been reported to occur together more fre- phase a screening questionnaire was mailed to random quently than expected [13]. At frst, several reviews did samples from the general population aged 20–84 years, not fnd out a clear evidence-based relationship between while in the clinical phase subjects reporting symptoms Chronic rhinosinusitis and GERD [13–15]. However, in suggestive of chronic bronchitis, asthma or rhinitis, as the last years the association between GERD and sinusi- well as a sample of subjects without respiratory symp- tis gained support. Two European studies found that the toms, were invited to a local Respiratory/Allergy Unit, in SNOT (Sino-Nasal Outcome Test) score signifcantly order to undergo interviews and clinical tests. In particu- increased among patients with GERD, suggesting a direct lar, participating subjects were administered a modifed role of GERD in the development of chronic rhinosinusi- version of the ECRHS (European Community Respiratory tis [10, 16]. A large cohort study based on Taiwan Health Health Survey) clinical questionnaire, including detailed Care Utilization database by Lin et al. [17] found that questions on socio-demographic characteristics, smoking the risk of developing chronic rhinosinusitis was more habits and other lifestyle factors, respiratory symptoms than doubled in cases with newly diagnosed GERD with and other disturbances, drug consumption [23; available respect to controls matched for sex, age and comorbidi- at www.geird .org]. In each center, the GEIRD study was ties. In a population-based Brazilian survey the diagnosis approved by the local ethics committee and written con- of gastritis/ulcer/gastroesophageal refux was associated sent was obtained from each participant. with higher prevalence of rhinosinusitis symptoms in Fifty-nine percent (17,972/30,349) of selected subjects multivariable analysis [18]. An Italian study on a small answered the screening questionnaire, while 2,945 sub- series undergoing both nasal cytology and esophageal jects out of 7,739 participated in the clinical visit between manometry and 24-h pH-impedance monitoring showed 2008 and 2014, yielding a participation rate of 40.1%. that NAR with neutrophils strongly correlated with higher acid exposure time and refuxes number [19]. On Nasal disorders the basis of this accumulating evidence, the International Subjects were classifed as having "rhinitis" if they Consensus Statement on Allergy and Rhinology: Rhi- answered afrmatively to at least one of the following nosinusitis [20] assigned grade B evidence to support the questions: "Do you have any nasal allergies including association between chronic rhinosinusitis and GERD, hay fever?", "During your lifetime have you ever had any although causation could not be clearly demonstrated. nasal allergies including hay fever?", "Have you ever had Te association between GERD and AR is more ques- a problem with sneezing, or a runny or a blocked nose tioned. Te recent International Consensus Statement when you did not have a cold or the fu?". Rhinitis was on Allergic Rhinitis does not even mention GERD at all further classifed as allergic rhinitis (AR) and non-allergic as a potential risk factor [21]. Te situation is complex, rhinitis (NAR), according
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