Secondary Logo

Journal Logo

COVID Reports

Prevalence of Anosmia in 10.157 Pediatric COVID-19 Cases

Multicenter Study from Turkey

Elvan-Tuz, Aysegul MD*; Karadag-Oncel, Eda MD, MSc*; Kiran, Sibel MD, PhD; Kanik-Yuksek, Saliha MD; Gulhan, Belgin MD; Hacimustafaoglu, Mustafa MD§; Ozdem-Alatas, Silem MD; Kuyucu, Necdet MD; Ozdemir, Halil MD**; Egil, Oguz MD††; Elmas-Bozdemir, Sefika MD‡‡; Polat, Meltem MD§§; Bursal-Duramaz, Burcu MD¶¶; Cem, Ela MD‖‖; Apaydin, Gozde MD***; Teksam, Ozlem MD;  on behalf of the TURK-COVID-19-Anosmia Study Group

Author Information
The Pediatric Infectious Disease Journal: June 2022 - Volume 41 - Issue 6 - p 473-477
doi: 10.1097/INF.0000000000003526

Abstract

COVID-19, caused by SARS-CoV-2, continues to spread rapidly around the world. Early detection and isolation of cases still remain important. While fever, cough, myalgia, and weakness are common symptoms of the disease, awareness has increased that anosmia and ageusia are specific findings.

In viral infections, anosmia may occur through the inflammatory reaction of the nasal mucosa and the development of rhinorrhea. However, many patients infected with SARS-CoV-2 experienced severe anosmia and ageusia without rhinorrhea or nasal congestion.1 The pathophysiology of anosmia is thought to be sensorineural inflammation of the olfactory neuroepithelium.2 Therefore, the anosmia seen in COVID-19 is a remarkable and disease-specific finding.

The prevalence of anosmia varies widely between studies. Currently, there is no clear data on how the frequency of anosmia changes depending on factors such as age, gender, clinical severity, and the relationship between different countries and ethnic populations. In this multicenter cohort study, we aimed to determine the prevalence of anosmia in pediatric cases with COVID-19 in our country and make an objective evaluation with a smell awareness questionnaire.

MATERIAL AND METHODS

Participants

This multicenter prospective cohort study was conducted between October 2020 and March 2021 with pediatric infection clinics from 37 centers located in 19 different cities of Turkey. Throughout the study period, cases 10–18 years old in whom SARS-CoV-2 was detected in respiratory samples by reverse transcriptase-polymerase chain reaction method were examined. It was planned to interview the cases with anosmia at admission and one month after the disease.

Study Design and Definitions

During the interviews at admission, age, gender, and other symptoms accompanying COVID-19 were recorded. COVID-19 clinical classification was made (asymptomatic, mild, moderate, severe, critical). The smell awareness questionnaire consisting of 20 questions was applied to the cases with anosmia.3,4 The questionnaire started with items that included awareness of smell and consisted of items that questioned smell acuity and smell-related behavioral characteristics. Afterward, the cases were informed that they would be called again one month later. One month later, the patients were interviewed by phone and the smell awareness questionnaire was applied for the second time. The answers to the questions were scored from 1 to 5. The responses were determined as follows, always (1 point), often (2 points), some time (3 points), rare (4 points), and never (5 points). In addition, the duration of anosmia, the onset time of anosmia, and whether there was any improvement in the findings at the end of one month were questioned. This study was approved by the Health Sciences University, Izmir Tepecik Training and Research Hospital Ethical Committee in accordance with the Helsinki Declaration (Decision number: 2020/14-70).

Statistical Analysis

Statistical data were analyzed with IBM SPSS for Windows version 25.0 (Chicago, IL). Values for numerical variables were given as median (interquartile range) (IQR) or mean ± standard deviation, depending on the normality distribution. Categorical variables were presented as numbers and percentages. Categorical variables were compared using the χ2 test. Wilcoxon test was used to compare the questionnaires. A P value of <0.05 was considered statistically significant for all predictions.

RESULTS

Characteristics of Participants With and Without Anosmia

Of the 10.157 patients with COVID-19, anosmia prevalence was determined 12.5% (n = 1266). Two-hundred-thirteen patients who could not be contacted for various reasons or did not agree to participate in the study were excluded. The remaining 1053 cases were included in the study. Of the 1053 cases, 643 (61.1%) were female and the median age of the cases was 190 (168–204) months. When the cases were analyzed according to age groups, 34.9% were between the ages of 10–14 and 65.1% were between the ages of 15–18. When evaluated in terms of clinical severity, 925 cases (87.8%) were mild, 126 (12%) were moderate, one (0.1%) were severe, and one (0.1%) were critical.

Of the 10.157 COVID-19 cases in our population, 8891 (87.5%) had no anosmia. When the COVID-19 cases without anosmia were analyzed, it was found that 49.6% of them were female. Female gender was found to be significantly more common in cases with anosmia (61.1% vs. 49.6%, P < 0.001). The median age of the cases without anosmia was 176 (152–196) months. When the cases were analyzed in terms of age groups, 52.3% were between the ages of 10–14 and 47.7% were between the ages of 15–18. It was observed that the cases with anosmia were older and the presence of anosmia was more common between the ages of 15–18 (P < 0.001, P < 0.001, respectively). Clinical severity data were available for 8590 of the cases without anosmia. Of these cases 1322 (15.5%) were asymptomatic, 6604 (76.9%) were mild, 546 (6.4%) were moderate, 102 (1.2%) were severe, and 16 (0.2%) were critical clinical severity (Table 1).

TABLE 1. - Characteristics of COVID-19 Patients Presenting With and Without Anosmia
Patients with Anosmia (n = 1053) Patients without Anosmia (n = 8891)
Age (months)* 190 (168–204) 176 (152–196)
Gender (female)** 643 (61.1) 4410 (49.6)
Clinical severity** n = 8590
Asymptomatic 0 (0) 1322 (15.5)
Mild 925 (87.8) 6604 (76.9)
Moderate 126 (12) 546 (6.4)
Severe 1 (0.1) 102 (1.2)
Critical 1 (0.1) 16 (0.2)
Anosmia (days)* 7 (3–14)
Onset of anosmia**
As the only symptom of COVID-19 84 (8)
Before general symptoms of COVID-19 172 (16.3)
At the same time as general symptoms of COVID-19 341 (32.4)
After general symptoms of COVID-19 456 (43.3)
Outcome of anosmia**
Regressed 965 (91.6)
Not regressed 88 (8.4)
Ageusia** 885 (84)
Ageusia (days)* 7 (3-14)
Onset of ageusia**
As the only symptom of COVID-19 with anosmia 57 (6.4)
Before general symptoms of COVID-19 173 (19.5)
At the same time as general symptoms of COVID-19 261 (29.5)
After general symptoms of COVID-19 394 (44.5)
Outcome of ageusia at one month**
Regressed 827 (93.4)
Not regressed 58 (6.6)
IQR, interquartile range.
*median (IQR).
**n, %.

Clinical Characteristics of Participants with Anosmia

While ageusia was accompanying in 885 (84%) of the cases, fatigue in 534 (50.7%) cases, cough in 466 (44.3%) cases, headache in 456 (43.3%) cases, fever in 449 (42.6%) cases, myalgia in 433 (41.1%) cases, and joint pain in 360 (34.2%) cases were other common symptoms. All symptoms and symptom durations of COVID-19 cases presenting with anosmia are shown in Table 2. When the duration of symptoms was examined, it was found that the median duration of anosmia was seven (IQR: 3–14) days. Anosmia was the only symptom in 84 (8%) of 1053 COVID-19 cases with anosmia. According to the onset times, anosmia was detected before general symptoms in 172 (16.3%) cases, concurrent with general symptoms in 341 (32.4%) cases, and after general symptoms in 456 (43.3%) cases. One month later, it was seen that there was no regression in the complaints of anosmia in 88 (8.4%) cases. The course of anosmia was compared with clinical severity. The cases were divided into two groups mild and moderate/severe/critical. While anosmia did not improve in 7.7% of cases in the mild clinical severity group, it was found that anosmia did not improve in 13.3% in the moderate/severe/critical clinical severity group and the difference between the groups was statistically significant (P = 0.04).

TABLE 2. - Other Symptoms of COVID-19 Patients Presenting with Anosmia
Symptom Symptom frequency (n, %) Symptom duration (days) median (IQR)
Ageusia 885 (84) 7 (3–14)
Weakness 534 (50.7) 5 (3–7)
Cough 466 (44.3) 4 (3–7)
Headache 456 (43.3) 4 (2–7)
Fever 449 (42.6) 2 (1–3)
Myalgia 433 (41.1) 4 (3–7)
Joint pain 360 (34.2) 4 (2–7)
Appetite loss 272 (25.8) 5 (3–7)
Nasal congestion 239 (22.7) 4 (3–7)
Rhinorrhea 183 (17.4) 3 (2–6)
Chest pain 160 (15.2) 3 (2–7)
Nausea and vomiting 149 (14.2) 3 (2–5)
Dyspnea 145 (13.8) 4 (2–7)
Diarrhea 143 (13.6) 2 (2–4)
Stomach ache 110 (10.4) 3 (2–5)
Hoarseness 81 (7.7) 4 (3–6)
Tinnitus 28 (2.7) 3 (2–6)
Hearing loss 4 (0.4) 2 (2–3)

Clinical Characteristics of Participants with Ageusia

Ageusia was present in 885 (84%) of 1053 participants with anosmia. When the duration of symptoms was examined, it was found that the median duration of ageusia was seven (IQR: 3–14) days. Ageusia was detected before general symptoms in 173 (19.5%) cases, simultaneously with general symptoms in 261 (29.5%) cases, and after general symptoms in 394 (44.5%) cases. One month later, it was seen that 58 (6.6%) patients did not regress in ageusia complaints (Table 1).

Smell Awareness Questionnaire

While the median value of the total score of the questionnaire applied to the cases at the time of admission was 94 (IQR: 80–100) points, the median value of the total score of the questionnaire applied one month later was 46 (IQR: 31–62) points. All questions in the smell awareness questionnaire and the scores of the participants are shown in Table, Supplemental Digital Content 1; https://links.lww.com/INF/E698. A total of 20 questions and scores in the questionnaire were compared according to admission and one month after the illness. At the time of admission, the scoring was higher than the scoring one month later (94 vs. 46, P < 0.001).

DISCUSSION

With this study, we have provided the examination of a large case series across Turkey. Anosmia and ageusia are specific symptoms seen in cases with COVID-19. Given the current pandemic, it is thought that the chance of detecting the disease will increase in the presence of sudden onset anosmia and ageusia. The importance of this situation is understood day by day and precautions are taken. So much so that the American Academy of Otolaryngology-Head and Neck Surgery recommended that people with sudden anosmia and ageusia isolate themselves in the absence of other respiratory symptoms such as nasal congestion and rhinorrhea.5 In countries where access to COVID-19 testing and resources are limited, these and similar recommendations are of great importance.

The prevalence of anosmia in COVID-19 patients varies widely between studies. In a systematic review of 27 publications that included a total of 19.424 COVID-19 patients, the prevalence of anosmia ranged from 4.23% to 98.33%.6 In our population, this rate was 12.46%. In an international multicenter study of 394 cases of COVID-19 involving children and adults, the incidence of anosmia was significantly higher in cases in Germany and France than in China.7 Age, regional variations, ethnic origin, and an insufficient number of cases in cross-sectional studies can be cited as the reasons for this variability.

In COVID-19 cases, anosmia is more common in women.8 Similarly, female gender was detected more frequently in cases with anosmia in our study.

The exact pathophysiology of anosmia and ageusia in COVID-19 has not yet been fully elucidated. It mainly focuses on three mechanisms. First, it is thought that inflammation of the olfactory mucosa may be triggered by a viral infection of the nasal mucosa. Second is thought to be caused by damage resulting in inhibition of olfactory signal transduction. The third mechanism is that this neurotropic virus follows the olfactory pathway to attack the olfactory cortex of the brain’s temporal lobe.9,10 In a meta-analysis, in studies where SARS-CoV-2 negative patients were the control group, anosmia was more common in SARS-CoV-2 positive individuals.11 This situation supports that anosmia has a specific place in COVID-19 disease.

While anosmia and ageusia due to nasal congestion or rhinorrhea are common in viral infections, the situation in COVID-19 is specific. Nasal congestion was detected in 22.7% of our cases, and rhinorrhea was found in 17.4%. This supports the hypothesis that different mechanisms are involved in COVID-19. In this study, in which we examined cases with anosmia and ageusia, the most common accompanying symptoms were fatigue (50.7%) and cough (44.3%). In a study examining the symptom profile of the disease for SARS-CoV-2 in the United Kingdom, the most common symptoms in school-age children were headache (62.2%) and fatigue (55.0%).12 In the meta-analysis examining both community-based children and hospital admissions, fever (47%) and cough (42%) were reported as the most common symptoms.13 Our population consisted of children with anosmia, although symptoms were similar to the COVID-19 case series.

The effects of symptoms accompanying anosmia on the severity, duration, and overall recovery rates of anosmia have been investigated in the literature. Patients with isolated anosmia have been found to have longer recovery times and more severe olfactory dysfunction than patients with anosmia accompanied by other clinical symptoms.8 We did not make such a comparison in our study. In future studies, this situation can be handled and clearer results can be revealed.

In our population, non-permanent hearing loss developed in four (0.4%) cases. In the literature, cases in the adult age group with hearing loss after anosmia and ageusia have been reported.14 In another study, hearing loss was found in 6.35% of COVID-19 cases.15 The effect of COVID-19 disease on the auditory system still remains unclear. Therefore, it is necessary to be careful in terms of other sensory deficits in COVID-19 cases.

In our study, anosmia and ageusia were frequently observed after general symptoms (43.3% and 44.5%, respectively). Anosmia and ageusia were detected at a low rate as the only symptom in COVID-19 cases (8%, 6.4%, respectively). Similarly, in the literature, anosmia, and ageusia were observed as the sole symptom in 10% and after the general symptoms in 53%.7 However, since the participants in our study were between the ages of 10–18, generalizing these rates to all COVID-19 cases may be misleading. Although anosmia and ageusia are specific symptoms, their detection late in the course of the disease can be seen as a disadvantage.

It has been reported that COVID-19-related anosmia is associated with a mild clinical course and a good prognosis. This mechanism is thought to help prevent both central neuroinvasion and viremia.16 In our study, it was seen that 87% of the cases were in the mild clinic. A study of critically ill patients with COVID-19 in the intensive care unit supports the existing hypothesis that anosmia is less common with increasing disease severity.17 On the other hand, in our cases with moderate/severe/critical clinical severity, we found that anosmia recovery rates were lower than mild. Based on the available data, it can be said that anosmia is often associated with a mild clinical course, and recovery rates decrease with worsening clinical severity.

The recovery process and prognosis of patients with anosmia are of critical importance. Postviral anosmia shows complete or partial recovery in about two weeks to several months, depending on the pathophysiology of the anosmia.18 In our cases, the median recovery times of anosmia and ageusia were seven days. In a study conducted with a large case series, the recovery time of anosmia was shorter in children than in adults.19 With this result, it can be thought that restoring olfactory function occurs faster in children than in adults. The short-term improvement seen in our cases also supports our conclusion. One month later, when the cases were questioned again, it was observed that anosmia resolved with a rate of 91.6%. This high rate is promising to show that patients have a low risk of permanent dysfunction. Cases whose symptoms do not improve should be referred to otolaryngology clinics. As a matter of fact, a case of severe acute respiratory syndrome (SARS) associated with anosmia that has been ongoing for two years has been reported in the literature.20

There is no definitive treatment regimen for anosmia associated with COVID-19. The British Rhinological Society consensus guidelines recommend nasal/systemic steroid and omega-3 supplementation in addition to olfactory exercises.21

This study had some limitations. Initially, subjects were called for anosmia evaluation one month later; but the follow-ups thereafter were not included in the study. By evaluating long-term follow-ups, the relationship between COVID-19 and anosmia can be examined in depth. Second, a qualitative research method was used for anosmia assessment. The use of quantitative research methods can provide a more objective assessment.

In conclusion, anosmia and ageusia are common symptoms in COVID-19 and maybe the only symptom in some cases. With the detection of these symptoms, it should be aimed to isolate COVID-19 cases in the early period and reduce the spread of infection. There are limited data on the prevalence of anosmia in children and adolescents. Also, such studies are important because the course of COVID-19 in children differs from adults. We aimed to contribute to the literature in this sense with this multicenter study that included a large number of cases. It should be aimed to enrich the literature with similar studies that include long-term follow-up of the cases.

ACKNOWLEDGMENTS

TURK-COVID-19-Anosmia Study Group: Ibrahim Cukurova, MD, Prof, (Health Sciences University Tepecik Training and Research Hospital, Izmir); Ozlem Mustafaoglu, MD, (Ankara City Hospital, Ankara); Ahmet Yasin Guney, MD, (Ankara City Hospital, Ankara); Emre Sahin, MD, (Uludag University Hospital, Bursa); Berfin Ozgokce Ozmen, MD, (Mersin University Hospital, Mersin); Mehtap Akca, MD, (Mersin University Hospital, Mersin); Goksel Vatansever, MD, (Ankara University Hospital, Ankara); Deniz Tekin, MD, Prof, (Ankara University Hospital, Ankara); Ayse Buyukcam, MD, (Gaziantep CG Obstetrics and Children’s Hospital, Gaziantep); Nur Ozcan, MD, (Bursa Dortcelik Children’s Hospital, Bursa); Suna Ozdem, MD, (Health Sciences University Dr Sami Ulus Training and Research Hospital, Ankara); Lida Bulbul, MD, (Bezmialem Vakif University Hospital, Istanbul); Sahika Sahinkaya, MD, (Health Sciences University Behcet Uz Training and Research Hospital, Izmir); Fatma Deniz Aygun, MD, (Istanbul University Cerrahpasa, Istanbul); Emre Gungor, MD, (Hacettepe University Hospital, Ankara); Asuman Demirbuga, MD, (Istanbul University Hospital, Istanbul); Metin Uysalol, MD, (Istanbul University Hospital, Istanbul); Burcu Ceylan Cura Yayla, MD, (Ankara Training and Research Hospital, Ankara); Kubra Aykac, MD, (Ankara Training and Research Hospital, Ankara); Ayse Tekin, MD, (Eskisehir City Hospital, Eskisehir); Ilknur Caglar, MD, (Aydin Gynecology and Pediatrics Hospital, Aydin); Sule Demir, MD, (Aydin Gynecology and Pediatrics Hospital, Aydin); Nimet Melis Bilen, MD, (Ege University Hospital, Izmir); Bilge Aldemir Kocabas, MD, (Health Sciences University Antalya Training and Research Hospital, Antalya); Gulperi Timurtas Dayar, MD, (Health Sciences University Antalya Training and Research Hospital, Antalya); Muhammet Kosker, MD, (Health Sciences University Antalya Training and Research Hospital, Antalya); Yalcin Kara, MD, (Osmangazi University Hospital, Eskisehir); Mahmut Can Kizil, MD, Osmangazi University Hospital, Eskisehir; Taylan Celik, MD, (Canakkale Onsekiz Mart University, Canakkale); Benhur Sirvan Cetin, MD, (Erciyes University Hospital, Kayseri); Yunus Emre Dogan, MD, (Erciyes University Hospital, Kayseri); Soner Sertan Kara, MD, (Aydin Adnan Menderes University, Aydin); Tugba Demir, MD, (Aydin Adnan Menderes University, Aydin); Semra Bayturan Sen, MD, (Manisa Celal Bayar University, Manisa); Alkan Bal, MD, (Manisa Celal Bayar University, Manisa); Ozge Metin Akcan, MD, (Necmettin Erbakan University, Meram Hospital, Konya); Mustafa Genceli, MD, (Necmettin Erbakan University, Meram Hospital, Konya); Ayse Karaaslan, MD, (Dr. Lütfi Kirdar Kartal Training and Research Hospital, Istanbul); Ceren Cetin, MD, (Dr. Lütfi Kirdar Kartal Training and Research Hospital, Istanbul); Ummuhan Cay, MD, (Cukurova University Hospital, Adana); Sevgen Tanir Basaranoglu, MD, (Firat University Hospital, Elazig); Esra Akyuz Ozkan, MD, (Ondokuz Mayis University Hospital, Samsun); Emine Hafize Erdeniz, MD, (Ondokuz Mayis University Hospital, Samsun); Ozlem Cakici, MD, (Kocaeli University Hospital, Kocaeli); Kamile Arikan, MD, (Buca Seyfi Demirsoy Training and Research Hospital, Izmir); Edanur Yesil, MD, (Mersin City Hospital, Mersin); Murat Sutcu, MD, (Istinye University Hospital, Istanbul); Manolya Kara, MD, (Istinye University Hospital, Istanbul); Ahmet Bolat, MD, (Ankara Gulhane Training and Research Hospital, Ankara); Zuhal Umit, MD, (Manisa City Hospital, Manisa); Hatice Uyanik Uygun, MD, (Adiyaman University Hospital, Adiyaman); Arife Ozer, MD, (Van Training and Research Hospital, Van); Ozden Turel, MD, (Bezmialem Vakif University Hospital, Istanbul); Zumrut Sahbudak Bal, MD, (Ege University Hospital, Izmir); Yasemin Ozsurekci, MD, (Hacettepe University Hospital, Ankara); Selda Hancerli Torun, MD, (Istanbul University Hospital, Istanbul); Ahu Kara Aksay, MD, (Health Sciences University Tepecik Training and Research Hospital, Izmir); Selim Oncel, MD, (Kocaeli University Hospital, Kocaeli); Omer Kilic, MD, (Osmangazi University Hospital, Eskisehir); Derya Alabaz, MD, (Cukurova University Hospital, Adana); Ergin Ciftci, MD, (Ankara University Hospital, Ankara); Nursen Belet, MD, (Dokuz Eylul University Hospital, İzmir); Ilker Devrim, MD, (Health Sciences University Behcet Uz Training and Research Hospital, Izmir); Haluk Cezmi Cokugras, MD, (Istanbul University Cerrahpasa, Istanbul); Zafer Kurugol, MD, (Ege University Hospital, Izmir); Dilek Yilmaz Ciftdogan, MD, (Health Sciences University Tepecik Training and Research Hospital, Izmir); Mehmet Turgut, MD, Adiyaman University Hospital, Adiyaman; Ates Kara, MD, (Hacettepe University Hospital, Ankara).

REFERENCES

1. Passali GC, Bentivoglio AR. Comment to the article “Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study”. Eur Arch Otorhinolaryngol. 2020;277:2391–2392.
2. Mak PQ, Chung KS, Wong JS, et al. Anosmia and Ageusia: not an uncommon presentation of COVID-19 infection in children and adolescents. Pediatr Infect Dis J. 2020;39:e199–e200.
3. Smeets MAM, Veldhuizen MG, Galle S, et al. Sense of smell disorder and health-related quality of life. Rehabil Psychol. 2009;54:404–412.
4. Kiran S. Oas odor awareness scale-modified Turkish version (OASmTR) and exposure and odor perception in hospital workers. In: 30th International Congress on Occupational Health Conference, Cancun, 2012, Mexico.
5. Anosmia H. Dysgeusia symptoms of coronavirus disease. American Academy of Otolaryngology. 2020. https://www.entnet.org/covid-19/anosmia/
6. Ibekwe TS, Fasunla AJ, Orimadegun AE. Systematic review and meta-analysis of smell and taste disorders in COVID-19. OTO Open. 2020;4:2473974X20957975.
7. Qiu C, Cui C, Hautefort C, et al. Olfactory and gustatory dysfunction as an early identifier of COVID-19 in adults and children: an international multicenter study. Otolaryngol Head Neck Surg. 2020;163:714–721.
8. Altundag A, Saatci O, Sanli DET, et al. The temporal course of COVID-19 anosmia and relation to other clinical symptoms. Eur Arch Otorhinolaryngol. 2021;278:1891–1897.
9. Wu Y, Xu X, Chen Z, et al. Nervous system involvement after infection with COVID-19 and other coronaviruses. Brain Behav Immun. 2020;87:18–22.
10. Keyhan SO, Fallahi HR, Cheshmi B. Dysosmia and dysgeusia due to the 2019 Novel Coronavirus; a hypothesis that needs further investigation. Maxillofac Plast Reconstr Surg. 2020;30:9.
11. Boscutti A, Delvecchio G, Pigoni A, et al. Olfactory and gustatory dysfunctions in SARS-CoV-2 infection: a systematic review. Brain Behav Immun Health. 2021;15:100268.
12. Molteni E, Sudre CH, Canas LS, et al. Illness duration and symptom profile in symptomatic UK school-aged children tested for SARS-CoV-2. Lancet Child Adolesc Health. 2021;5:708–718.
13. Li B, Zhang S, Zhang R, et al. Epidemiological and clinical characteristics of COVID-19 in children: a systematic review and meta-analysis. Front Pediatr. 2020;8:591132.
14. Jacob J, Flannery W, Mostert C. Novel ENT triad of anosmia, ageusia and hearing impairment in COVID-19. Intern Med J. 2020;50:1155.
15. Gosavi S, Nagarajan S, Shah NJ, et al. ENT symptomology in active COVID-19 patients in our tertiary care centre. Indian J Otolaryngol Head Neck Surg. 2021;18:1–6.
16. Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study. Eur Arch Otorhinolaryngol. 2020;277:2251–2261.
17. Sayin P, Altinay M, Cinar AS, et al. Taste and smell impairment in critically ill patients with COVID-19: an intensive care unit study. Ear Nose Throat J. 2021;100:174–179.
18. Gane SB, Kelly C, Hopkins C. Isolated sudden onset anosmia in COVID-19 infection. A novel syndrome? Rhinology. 2020;58:299–301.
19. Mizrahi B, Shilo S, Rossman H, et al. Longitudinal symptom dynamics of COVID-19 infection. Nat Commun. 2020;11:6208.
20. Hwang CS. Olfactory neuropathy in severe acute respiratory syndrome: report of A case. Acta Neurol Taiwan. 2006;15:26–28.
21. Hopkins C, Alanin M, Philpott C, et al. Management of new onset loss of sense of smell during the COVID-19 pandemic - BRS Consensus Guidelines. Clin Otolaryngol. 2021;46:16–22.
Keywords:

anosmia; ageusia; COVID-19; children

Supplemental Digital Content

Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.