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Clinical Signs in Allergic Rhinitis Patients at Dr. Hasan Sadikin General Hospital Bandung 2017–2021

Background: The clinical diagnosis of allergic rhinitis requires comprehensive data from the history and physical examination. Despite being a substantial component of the diagnosis of allergic rhinitis, there is a paucity of studies about clinical signs of allergic rhinitis in Indonesia. This study aimed to describe the clinical signs in allergic rhinitis patients at Dr. Hasan Sadikin General Hospital Bandung. Methods: This cross-sectional study was conducted at Dr. Hasan Sadikin General Hospital Bandung in 2021, including secondary data of patients with allergic rhinitis from medical records registered from 2017 to 2021. Data on the characteristics, clinical signs, and allergic rhinitis comorbidities were collected and presented in tables. Results: The most common clinical sign was turbinate hypertrophy (74%), followed by pale nasal mucosa (59%) and clear nasal discharge (59%). The most prevalent comorbidities were chronic rhinosinusitis, adenoid hypertrophy, and asthma. Conclusion: The clinical signs observed from allergic rhinitis patients may vary, with the most common findings, including nasal turbinate hypertrophy, pale nasal mucosa, and clear nasal discharge. The findings may help clinicians to diagnose allergic rhinitis needed for therapy management.


Introduction
Allergic rhinitis is a disorder of nasal mucosa due to exposure to allergen particles that cause inflammation mediated by Immunoglobulin E (IgE). 1 The symptoms include nasal congestion, runny nose, sneezing, an itchy nose, and loss of smell when the nasal mucosa is exposed to allergens. Allergic rhinitis affects about 10% to 30% of the world's population. Based on a previous study, the prevalence of allergic rhinitis in Indonesia is 38.2%. 2 The diagnosis of allergic rhinitis is made based on history taking, physical examination, and supporting examination. 1 A complete history is required to look for potential triggers, nasal symptoms, and a family history of atopy. Clinical signs observed from physical examination act as objective evidence to rule out the differential diagnosis and may indicate the presence of comorbidities. Physical examination is performed by anterior rhinoscopy, which shows hypertrophy and pale inferior turbinate mucosa with clear secretions. Nasal endoscopy can be performed to assess the nasal cavity in more detail and support the diagnosis of allergic rhinitis. 3,4 The comorbidities include asthma, conjunctivitis, chronic rhinosinusitis with or without nasal polyps, otitis media with effusion, and adenoid hypertrophy. Those comorbidities cause sleep disturbance which acts as factors that worsen the quality of life if not given the appropriate treatment. 5 Definitive diagnosis is made by detecting allergen-specific IgE or the skin prick test. 6 The clinical diagnosis of allergic rhinitis, which is established as a prerequisite for appropriate treatment, requires comprehensive data from the history and physical examination. The inclusion criteria in this study were patients diagnosed with allergic rhinitis confirmed by a skin prick test, while the exclusion criteria were incomplete or missing medical records. The study variables were age, gender, family history of atopic disease, classification, cardinal symptoms, physical findings, and comorbidities. The collected data were analyzed using Microsoft Excel 2020 software to calculate the frequency of findings and presented in tables.

Results
Out of 463 patients with allergic rhinitis, 260 were included. The distribution of gender, age groups, and family history of the atopic disease was provided in Table 1. The classification of allergic rhinitis was described in Table 2 based on the ARIA-WHO guidelines. The most prevalent classification was moderate-severe persistent allergic rhinitis (45%), and the least prevalent was moderate-severe intermittent (4%).

Discussion
In the present study, the number of the female with allergic rhinitis patients was higher than that of males. The higher prevalence of female allergic rhinitis patients might occur due to estrogen and progesterone, which increase mast cell and IgE activity, making females more susceptible to atopic diseases such as allergic rhinitis and asthma. 7 The most prominent age groups were 10-19 and 20-29 year, who are still in school-age and productive age. Allergic rhinitis in both age groups impacts decreased productivity due to impaired concentration at school or work caused by the symptoms experienced, prompting patients to seek help from health facilities. 1,6 Many studies have shown that a family history of atopy is a risk factor for allergic rhinitis. A study in Sweden concluded that children born to parents with allergy have an increased 2-9 folds risk of allergic rhinitis. 8 Another study on Turkish adolescents with allergic rhinitis showed that 53% of the study population had at least 1 parent with atopy. 9 Similarly, a study in Indonesia has shown that 54% of cases present with an atopic family history. 2 These data were consistent with the results of our study, where nearly half (41%) of the patients had a family history of atopic disease. The classification of persistent moderatesevere allergy was the most common form in our study, similar to the previous studies conducted in clinical settings. 5,10 The reduced quality of life in patients with moderate-severe persistent allergic rhinitis might have caused the patients to be more likely to seek medical therapy than patients with milder allergic rhinitis classifications. 5 Cardinal symptoms of allergic rhinitis include nasal congestion, runny nose, sneezing, and itchy nose. 1 In a study involving 979 allergic rhinitis patients in France showed that nasal congestion was found in 82% of patients, followed by the runny nose (89%), sneezing (82%), and itchy nose (68%). 10 These were consistent with our study. The discrepancy between some studies with others could be explained by the varied symptoms of allergic rhinitis and comorbidities the study subjects might have.
The anterior rhinoscopy examination showed inferior turbinate hypertrophy, clear secretions, and pale mucosa in most study samples. Inflammatory mediators released by mast cells cause interstitial edema of the nasal mucosa, resulting in turbinate hypertrophy. 11 A study in Tanzania on 193 allergic rhinitis patients noted concha hypertrophy (69%), and another study in North Vietnam found turbinate hypertrophy (70%). 12,13 The mechanisms of increased watery nasal secretions include histamine-induced mucosal gland hyperactivity and plasma leakage. 11 Clear and watery nasal discharge was observed in 59%; however, the number of patients who complained of a runny nose was quite high (81%). The difference might occur due to patients with intermittent allergic rhinitis or patients who had received previous treatment, which allowed the secretions to be not visible at the time of the examination. A pale mucosal color caused by chronic inflammation of the nasal mucosa is associated with the level of eosinophil infiltration, which is a hallmark of allergic rhinitis. A study in Japan showed that the proportion of pink or normal mucosal color was 57%, and pale was 43%. 14 However, the study did not include the diagnosis of allergic rhinitis as an inclusion criterion that the subjects might not had before the examination. 14 In contrast to the study, our study was conducted on patients diagnosed with allergic rhinitis, and the most common color of the mucosa was pale blue (59%). The subjectivity in determining the mucosa color might have affected the results of both studies.
This study included the results of ear and oropharynx examinations. A small proportion of patients in this study showed ear membrane perforation (8%) and ear discharge (3%) which could be associated with chronic suppurative otitis media. Previous studies have shown that allergic rhinitis is a risk factor for chronic suppurative otitis media. The mechanism involved is nasal mucosa inflammation of allergic rhinitis patients can cause eustachian tube dysfunction, making it easier for acute infections to recur and inflammatory response of the middle ear mucosa to the allergens occur as in nasal mucosa. 15,16 Tonsil hypertrophy was found in 31 cases (12%), with grade 2 (9%) being the most common compared with grade 3 (2%) or 4 (1%). A study in Italy 17 has shown that children with persistent upper airway obstruction might be due to inflammation as allergen stimulation increases the risk of mild tonsillar hypertrophy but decreases the risk of severe tonsillar hypertrophy (grades 3 and 4). The turbinate hypertrophy possibly in allergic rhinitis can prevent allergens from reaching the tonsils and stimulate further hypertrophy. 17 The nasal endoscopic examination provides a more detailed evaluation of the nasal cavity than the anterior rhinoscopy. 1,18 Nasal endoscopic examination in this study showed inferior turbinate hypertrophy (82%) and clear secretions (78%), and these numbers are lesser found in physical examination. The limited scope of anterior rhinoscopy might explain these differences compared to nasal endoscopy. The examination of anterior rhinoscopy and nasal endoscopy were done on different days, which allowed the symptoms to improve or worsen, and symptoms of allergic rhinitis may appear intermittently. Nasal endoscopic examination in this study included an assessment of the osteomeatal complex. There was hypertrophy of the middle turbinate (20%), edema of the uncinate process (42%), and narrowing of the middle meatus (36%) that could play a role in the mechanism of chronic rhinosinusitis by impairing the drainage of the frontal, maxillary, and anterior ethmoid sinuses. 19 Nasal endoscopy can also be performed to detect comorbidities such as adenoid hypertrophy and nasal polyps in patients. 18 Allergic rhinitis must include the detection of comorbidities that can worsen the patient's quality of life if not treated appropriately. 4,5 The most frequent comorbidity found in this study was chronic rhinosinusitis without nasal polyps (53%), followed by adenoid hypertrophy (23%), asthma (11%), chronic rhinosinusitis with polyps (10%), and chronic suppurative otitis media (3%). A previous study conducted in Bandung, Indonesia, found that rhinosinusitis (50%), nasal polyps (25%), and asthma (10%) were the most prevalent comorbidities. 20 Another study conducted in Dar es Salam, Tanzania, showed the most common comorbid was adenoid hypertrophy (31%), followed by nasal polyps (14%), sinusitis (9%), and otitis media with effusion (9%). 12 The high proportion of comorbidities in the present study could be caused by the research location, Dr. Hasan Sadikin General Hospital Bandung, which is a top referral hospital in West Java Province, so patients tend to have more severe diseases. The difference in the proportion of comorbidities in the mentioned studies could be related to geographic factors and the multifactorial nature of the comorbidities.
This research, however, is subject to several limitations. The data presented in this study were taken from medical records dependent on the extent of the physician's assessment of the patients. Nevertheless, some clinical signs of allergic rhinitis were not assessed and therefore not recorded, for examples clinical signs such as adenoid facies, Dennie-morgan lines, and transverse nasal folds that may be present in allergic rhinitis patients. Another limitation came from the large number of medical records that could not be included in this study. Further studies are suggested to include clinical signs that were not available in this study and to be carried out in a larger population to obtain a more precise result.
To conclude, the clinical signs observed from allergic rhinitis patients may vary with the most common findings including nasal turbinate hypertrophy, pale nasal mucosa, and clear nasal discharge. The findings may help clinicians to diagnose allergic rhinitis needed for therapy management.