ENT pediatric infection diseases and its relationship with COVID-19. Results of a retrospective cohort study in Madrid, Spain

Abstract

Introduction

During the COVID-19 pandemic, ENT infections decreased but became more severe when combined with COVID-19. Post-pandemic, there has been a notable rise in ENT infections globally, particularly ear infections. In our region, we observed an increase in complicated pediatric ENT infections requiring urgent surgical intervention after the end of preventive measures. This study investigates the changes in ENT infection profiles in Madrid, Spain, following the pandemic.

Material and methods

We analyzed data from children who underwent urgent ENT surgical interventions at a Spanish tertiary hospital between January 2018 and December 2023. The data was divided into three groups: pre-pandemic (1st group), during the pandemic with preventive measures (2nd group), and post-pandemic after the removal of these measures (3rd group). Variables included demographics, clinical data, imaging, treatment, and hospitalization duration.

Results

The study involved 87 children (58.6% male) with a mean age of 6.4 years. There was a significant overall increase in ENT infections in the 3rd group compared to the 1st and 2nd groups (p = 0.036). Specifically, ear infections increased significantly after the removal of social measures (p = 0.033). In the 3rd group, Streptococcus pyogenes infections increased (p = 0.028), with Amoxicillin becoming the predominant treatment (p = 0.047), as opposed to Amoxicillin-clavulanic acid used for Fusobacterium in earlier periods (p = 0.00).

Discussion and conclusion

The pandemic has shifted the ENT infection profile, with increased ear infections and a rise in Group A streptococcus post-pandemic. This underscores the need for updated treatment strategies for pediatric ENT infections.

Resumen

Introducción

Durante la pandemia COVID-19, las infecciones ORL disminuyeron, pero se volvieron más graves cuando se combinaban con COVID-19. Tras la pandemia, ha habido un aumento notable en las infecciones ORL a nivel global, particularmente en infecciones otológicas. En nuestra región, hemos observado un incremento en las infecciones ORL pediátricas complicadas que requirieron intervención quirúrgica urgente tras la eliminación de las medidas preventivas sociales. El objetivo de este estudio es investigar el cambio en el perfil de infecciones ORL en Madrid (España) tras la pandemia.

Material y métodos

Analizamos los datos de aquellos niños que se sometieron a intervenciones quirúrgicas urgentes por infecciones ORL en un hospital terciario español entre enero de 2018 y diciembre de 2023. Los datos se dividieron en tres grupos: pre-pandemia (1º grupo), durante la pandemia con medidas preventivas (2º grupo) y post-pandemia tras la eliminación de estas medidas (3º grupo). Las variables analizadas incluyeron datos demográficos, clínicos, pruebas de imagen, tratamiento utilizado y tiempo de hospitalización.

Resultados

El estudio involucró a 87 niños (58,6% varones) con una edad media de 6,4 años. Hubo un aumento significativo en las infecciones ORL en el 3º grupo en comparación con los grupos 1º y 2º (p = 0.036). Específicamente, las infecciones otológicas aumentaron significativamente después de la eliminación de las medidas sociales (p = 0.033). En el 3º grupo, las infecciones por Streptococcus pyogenes aumentaron (p = 0.028), con la Amoxicilina convirtiéndose en el tratamiento predominante (p = 0.047), a diferencia de la Amoxicilina-ácido clavulánico que se utilizó para Fusobacterium en los periodos anteriores (p = 0.00).

Discusión y conclusion

La pandemia ha cambiado el perfil de las infecciones ORL, con un aumento en las infecciones otológicas y un incremento en el Streptococcus del grupo A post-pandemia. Esto subraya la necesidad de actualizar las estrategias de tratamiento para las infecciones ORL pediátricas.

Key points

• 1

  Increased ENT Infections Post-Pandemic: There has been a significant rise in ENT infections, particularly ear infections, in the post-pandemic period compared to before and during the pandemic.

• 2

  Shift in Pathogens: Post-pandemic, there has been a notable increase in infections caused by Streptococcus pyogenes, contrasting with the predominance of Fusobacterium during the pandemic.

• 3

  Change in Treatment Trends: The use of Amoxicillin has increased significantly after the pandemic, replacing Amoxicillin-clavulanic acid which was more commonly used during the pandemic.

• 4

  Higher Incidence of Severe Infections: The incidence of complicated ENT infections requiring urgent surgical intervention has risen since the removal of preventive measures.

• 5

  Need for Updated Treatment Strategies: The observed changes in infection profiles and treatment patterns highlight the necessity for adapting pediatric ENT treatment strategies to address the new trends post-pandemic.

Introduction

After the worldwide spread of the SARS-CoV-2 infection beginning on December 2019, the World Health Organization declared the appearance of COVID-19 pandemic on March 2020. Precisely, Spain and in particular, Madrid, was a really highly affected area; subsequently, preventive measures were imposed including social distance, mask use and promotion of hand hygiene, among others.¹ In our country, the alarm state was set from March until June 2020, which resulted in the closure of schools, reduction of essential jobs and limitation of movements, in order to prevent transmission of COVID-19.

As a result of these social measures, there was not only a decline in COVID-19 cases, but hospitals around the world also observed a decrease in upper respiratory tract infections.² However, it has also been demonstrated that the severity of ENT infections can increase when there is a co-infection with COVID-19.³

Few reports have already addressed post-pandemic ENT profile infections. Usually, deep neck infections are the most commonly found, followed by ear and lastly nasal infections.^4,5 Oppositely to this fact, it has already been reported by Galli et al. an increase in number of ENT infections after COVID-19 pandemic, principally at the expense of otologic complications.⁶ Similarly, in our experience, we have noticed a rise in surgical ENT complications after abolishment of social preventive measures.

Therefore, the aim of this study is to investigate whether there is a change in the upper respiratory tract infection profile after COVID-19 pandemic.

Material and methods

Ethical considerations

This study was approved by the Committee for the Protection of Human Subjects of the Gregorio Marañon University Hospital (ORLHGUGM_II).

Study design

This is a single-institution retrospective cohort study encompassing all pediatric patients who underwent an urgent ENT surgery at a referral tertiary hospital in Madrid, from January 2018 to December 2023.

Patients

All surgical records between January 2018 and December 2023 were examined.

We included patients aged 0 to 16 years who required urgent surgery performed by the on-call otolaryngologist due to complications from ENT infections. These cases were deemed urgent due to the patients' poor general condition and/or laboratory findings, and were considered to require resolution within the first 24 h following their visit to the emergency room. There were no exclusion criteria.

We developed a database including demographics (age and gender), ENT medical record, diagnosis, laboratory tests, radiological and microbiological findings, medical and surgical treatment performed, time of hospitalization (including intensive care unit) and surgical complications, among others.

For statistical analysis, we clustered our sample in three groups, according to COVID-19 pandemic and the preventive measures established by the National Government: 1^st group- pre-pandemic (January 2018–May 2020), 2^nd group- imposed COVID-19 preventive measures (June 2020–February 2022) and 3^rd group- abolished COVID- 19 preventive measures (March 2022–December 2023).

Severity infection classification

As a comparative variable among groups we labelled each infection complication in mild or severe according to clinical status, imaging diagnosis and surgery required.

In deep neck complications, we classified peritonsilar abscess (transoral surgery) as mild infection while parapharyngeal, retropharyngeal, parotid abscess and facial necrotizing fascitis (cervical surgery) as severe infection.

Regarding ear infections, we distributed them in mild infections: mastoiditis (exclusively treated with myringotomy ± tympanostomy tube), acute otitis media causing facial palsy (only treated with myringotomy ± tympanostomy tube) and severe infections: subperiosteal abscess and sigmoid sinus thrombosis (mastoidectomy).

Lastly, we clustered rhinosinusitis complications according to Chandler classification, separating Chandler 1 and 2 as mild infections and Chandler ≥ 3 as severe complications. Moreover, nasal and septal abscesses (endoscopic drainage) were classified as mild infections.

Statistical analysis

Data analysis was conducted using the SPSS v.25 software (IBM, Armonk, NY).

Descriptive analysis was performed. Continuous variables were described as mean ± standard deviation (SD) and those qualitative as percentages.

Analytical statistics were executed. Normality test (Shapiro Wilk and Kolmogorov- Smirnov) were performed, showing a non-normal distribution for all analyzed variables, except microorganisms. Univariate and multivariate analysis were conducted. U Mann-Whitney and Kruskal Wallis test were used to compare most of quantitative variables. A paired t test was used to compare normal distribution-quantitative variables. A chi-square test (χ²) or Fisher exact test were used to compare qualitative variables. Correlation among variables was calculated with the Spearman test. A P-value of 0.05 was used to assess statistical significance.

Results

Incidence (Fig. 1)

A highlighted increase in ENT pediatric infections was observed during the 3^rd period, with an incidence of 2.13 cases/month, doubling 1^st (0.9 cases/month) and 2^nd period rate (0.66 cases/month).

Figure 1.

Incidence of ENT pediatric surgical infections before, during and after introduction of COVID-19 measures.

Curiously, the peak of incidence was not seen during winter months but in June of 2023 (n = 6).

Demographics (Table 1)

A total of 87 pediatric patients were included in our study. Regarding COVID-19 distribution, 29.9% patients (n = 26) belonged to the 1^st group, 16.1% (n = 14) to the 2^nd and 54% (n = 47) to the 3^rd. The overall mean age was 6.4 years) and the median 5 years old. Of them, 58.6% children (n = 51) were male and the remaining 41.6% patients (n = 36) female.

Table 1.

Demographics of children with ENT surgical infections, grouped by time of presentation before, during and after introduction of COVID-19 measures (1^st period: January 2018–May 2020, 2^nd period: June 2020–February 2022, 3^rd period: March 2022–December 2023).

Variable	1^st group	2^nd group	3^rd group	P value
Total cases (%)	26 (29.9)	14(16.1)	47(54)	–
Period studied (months)	29	21	22	–
Sex n (%)
Male	19 (73.1)	6 (42.9)	26 (55.3)	0.143
Female	7 (26.9)	8 (57.1)	21 (44.7)
Age (Mean ± SD)	6,66 (±0,97)	8,61(±1,32)	5,58(±0,72)	0.085

SD = Standard deviation.

Diagnosis (Table 2)

According to ENT area, deep neck infections were the most commonly found (49.4%), followed by ear (42.5%) and nose (8.1%) complications considering the overall sample. However, analyzing each section separately, we see a progressive decrease of deep neck infections (1^st: 66.7%, 2^nd: 50% and 3^rd: 39.1%) and oppositely an increase of ear infections (1^st: 25.9%, 2^nd: 28.6% and 3^rd period: 56.5%), although only statistically significant the second statement (p = 0.033).

Table 2.

Diagnosis and complementary tests variables of the sample, clustered in the 3 groups.

Variable	1^st group	2^nd group	3^rd group	Total	P value
Location n (%)					0.036
Ear	7 (26.9)	4 (28.6)	22 (46.8)	33(37.9)	0.033
Nose	2 (7.7)	3 (21.4)	4 (8.5)	9(10.3)	0.457
Deep neck	17 (65.4)	7 (50)	21 (44.7)	45(51.7)	0.235
ENT historical record n (%)
Yes	4 (15.4)	1 (7.1)	4 (8.5)	9 (10.3)	0.439
No	22 (84.6)	13 (92.9)	43 (91.5)	78(89.7)
Previous PCP diagnosis n (%)
Yes	16 (61.5)	8 (47.1)	20 (42.6)	44(50.6)	0.464
No	10 (38.5)	6 (42.9)	27 (57.4)	43(49.4)
Diagnosis n (%)
Mastoiditis	3 (11.5)	4(28.6)	15(31.9)	22(25.3)	0.388
Subperiosteal abscess	2 (7.7)	0(0)	4(8.5)	6(6.9)
SS thrombosis	0(0)	0(0)	1(2.1)	1(1.1)
Facial palsy + AOM	2(7.7)	0(0)	2(4.3)	4(4.6)
Chandler 2	1(3.8)	0(0)	0(0)	1(1.1)
Chandler 3	1(3.8)	2(14.3)	3(6.4)	6(6.9)
Septal abscess	0(0)	1(7.1)	0(0)	1(1.1)
Vestibule abscess	0(0)	0(0)	1(2.1)	1(1.1)
Peritonsillar abscess	13(50)	7(50)	15(31.9)	35(40.2)
RA	3(11.5)	0(0)	2(4.3)	5(5.7)
PA	1(3.8)	0(0)	1(2.1)	2(2.3)
Facial cellulitis	0(0)	0(0)	2(4.3)	2(2.3)
Parotid abscess	0(0)	0(0)	1(2.1)	1(1.1)
Severity n (%)
Mild	20 (76.9)	12 (85.7)	34 (72.3)	66(75.9)	0.584
Severe	6 (23.1)	2 (14.3)	13 (27.7)	21(24.1)
Blood test mean value
White cells (109/l)	15186	17930	14413		0.264
C- reactive protein (mg/l)	8.03	7.12	7.74		0.909
Imaging test n (%)
Yes	17 (65,4)	10 (72.4)	32 (68.1)		0.925
No	9 (34.6)	4 (28.6)	15 (31.9)

PCP = Primary care physician. AOM = Acute otitis media. SS = Sigmoid sinus. RA = Retropharyngeal abscess. Parapharyngeal abscess = PA.

Specifically, the most frequent diagnosis was peritonsillar abscess (37.9%) followed by mastoiditis (29.9%) and subperiosteal abscess of the orbit (Chandler 3) (6.9%).

Half of patients (50.6%) were firstly diagnosed by Primary Care Pediatrician of a non-complicated ENT infection and the remaining 49.4% were directly diagnosed by the on-call Otorhinolaryngologist of a complicated ENT infection. According to children medical record, only 10.3% children did have a previous otolaryngology diagnosis, including chronic rhinosinusitis and recurrent tonsillitis.

While considering severity of the infection, 55% of severe patients were diagnosed postpandemic, however the proportion of complicated infections was similar in the 3 groups (1^st: 25.9%, 2^nd: 14.3% and 3^rd: 23.9%).

Complementary tests (Table 2)

In relation to imaging tests, 32.2% patients underwent an imaging test: computed tomography (92.9%), echography (10.7%) and X Ray (7.1%). 3 patients required 2 or more simultaneous imaging tests. As for blood test results, white cell counts and C reactive protein value were similar in the 3 groups (p = 0.264 and 0.909).

Microbiology (Table 3)

Microbiology sample was taken in 83.9% of patients. Of these, one or more microorganisms were cultured in 79.3% of cases. Among all, Streptococcus pyogenes (29.9%) was the most common pathogen found in the surgical samples. Staphylococcus aureus, Fusobacterium and other streptococci were also frequently found (19.5%,13.8% and 17.2% respectively).

Table 3.

Microbiology of the sample, divided in the 3 groups.

Variable	1^st group	2^nd group	3^rd group	Total	P value
Organism sample (%)
No sample taken	5 (19.2)	3 (21.4)	6 (12.8)	14(16,1)	0.65
No organism cultured	0 (0)	0 (0)	4 (8.5)	4(4.6)	0.078
1 organism positive	13 (50)	7 (50)	25 (53.2)	45(51.7)	0.995
> 1 organism positive	8 (30.8)	14 (28.6)	12 (25.5)	34(39.1)	0.961
Microorganism n (%)
Streptococcus pyogenes	8(30.9)	0(0)	16(34)	24(27.6)	0.028
Other streptococci	3(11.5)	2(14.3)	10(21.3)	15(17.2)	0.039
Haemophilus	3(11.4)	0(0)	2(4.3)	5(5.7)	0.583
Staphylococcus aureus	4(15.4)	6(42.9)	7(14.9)	17(19.5)	0.056
Fusobacterium	5(19.2)	6(42.9)	1(2.1)	12(13.8)	0.001
Eikenella	2(7.7)	1(7.1)	2(4.3)	5(5.7)	0.809
Prevotella	1(3.8)	1(7.1)	3(6.4)	5(5.7)	0.871
Parvimonas	1(3.8)	1(7.1)	2(4.3)	4(4.6)	0.809
Corynebacterium	0(0)	1(7.1)	5(10.6)	6(6.9)	0.157
Actynomices	1(3.8)	0(0)	2(4.3)	3(3.4)	0.583
Other	3(11.5)	0(0)	11(23.4)	14(16.1)	0.039

Aspects of the cohort significantly differed between periods (Table 3): 3^rd period group had a higher proportion Streptococcus pyogenes infections(p = 0.028), other streptococci infections (p = 0.039) and minor pathogens (principally anaerobes (p = 0.00)) while in 2^nd group Fusobacterium prevailed (p = 0.001).

Treatment (Table 4)

42.5% patients of the sample had recorded a previous antibiotic treatment administered by primary care or emergency care physicians.

Table 4.

Medical and surgical management of children of the sample.

Variable	1^st group	2^nd group	3^rd group	Total	P value
Previous antibiotic n (%)
Yes	12(50)	6(46.2)	16(34)	37(42.5)	0.749
No	12(50)	7(53.8))	31(66)	50(57.5)
IV treatment n (%)
AC	23(88.5)	12(85.7)	32(68.1)	67(77)	0.098
AC + metronidazole	0(0)	2(14.3)	4(8.5)	6(6.9)	0.09
CC	1(3.8)	0(0)	3(6.4)	4(4.6)	0.436
Ampicillin	2(7.7)	0(0)	2(4.3)	4(4.6)	0.405
Cefotaxime	0(0)	0(0)	2(4.3))	2(2.3)	0.286
VCM	0(0)	0(0)	2(4.3)	2(2.3)	0.286
Vancomycin	0(0)	0(0)	1(2.1)	1(1.1)	0.538
AC + clindamycin	0(0)	0(0)	1(2.1)	1(1.1)	0.538
Surgery n (%)
Myringotomy	1(3.8)	0(0)	1(2.1)	2(2.3)	0.641
Ear drainage tube	4(15.4)	4(28.6%)	17(36.2)	25(28.7)	0.171
Mastoidectomy	1(3.8)	0(0)	3(6.4)	4(4.6)	0.395
SA drainage	0(0)	0(0)	1(2.1)	1(1.1)	0.538
ESS	2(7.7)	1(7.1)	4(8.5)	7(8)	0.983
Combined approach	0(0)	2(14.3)	0(0)	2(2.3)	0.023
Transoral drainage	17(65.4)	7(50)	18(38.3)	42(48.3)	0.085
Cervical approach	0(0)	0(0)	3(6.4)	3(3.4)	0.151
Time of hospitalization Mean ± SD	3.73(±3.82)	4.71(±4.58)	3.55(±2.98)	3.79(±3.5)	0.55
Intensive care surveillance n (%)	1(3.8)	2(14.3)	1(2.1)	4(4.6)	0.245
Oral treatment n (%)
AC	25(96.2)	12(85.7)	35(74.5)	72(82.8)	0.028
Amoxicillin	1(3.8)	2(14.3)	11(23.4)	14(16.1)	0.047
ML	0(0)	0(0)	1(2.1)	1(1.1)	0.538
Treatment duration Mean ± SD	13.65(±6.6)	13.15(±6.9)	12.47(±5.3)	12.93(±6)	0.964
Readmission n (%)	2(7.7)	1(7.1)	1(1.1)	4(4.6)	0.481
Reintervention n (%)Mastoidectomy	2(7.7)	1(7.1)	1(1.1)	4(4.6)	0.691
Complications n (%)Sd Lemierre	0(0)	1(100)	0(0)	1(1.1)	0.246

AC: Amoxicillin-clavulanic acid. CC = Cefotaxime + clindamycin. VCM = Vancomycin + ceftriaxone + metronidazole. SA = Subperiosteal abscess. ESS = Endoscopic sinus surgery. IV = intravenous. ML = Metronidazole + levofloxacine.

After being evaluated by the Otorhinolaryngologist, medical treatment was agreed with Infectious Diseases Pediatricians. Amoxicillin with clavulanic acid was the choice treatment in the overall sample (75.6% of patients) during the 3 periods, usually accompanied by oral or intravenous steroids (44.1% of patients). If divided according to areas (Table 5), Amoxicillin- clavulanic acid in monotherapy is still the preferred treatment (ear: 78.4%, nose:100% and deep neck: 82.8%). Other antibiotics such as Cephalosporins (12.1%) in otologic infections or Metronidazol (13.13%) for deep neck complications are used as well. Moreover, topical treatment was equally important including nasal corticosteroids or antibiotic drops, among others.

Table 5.

Microbiology and treatment according to ENT areas.

Microorganism n (%)	Ear	Nose	Deep neck
No sample	5 (15.2)	0 (0)	9 (20)
No organism cultured	1 (3)	2 (22.2)	1 (2.2)
Streptococcus pyogenes	12 (36.4)	0 (0)	14 (31.1)
Other streptococci	4 (12.1)	2 (22.2)	9 (20)
Haemophilus	1 (3)	0 (0)	2 (4.4)
Staphylococcus aureus	7 (21.2)	5 (55.6)	5 (11.1)
Fusobacterium	2 (6.1)	1 (11.1)	9 (20)
Eikenella	0 (0)	2 (22.2)	3 (6.7)
Prevotella	0 (0)	0 (0)	5 (11.1)
Parvimonas	0 (0)	0 (0)	4 (8.9)
Corynebacterium	2 (6.1)	1 (11.1)	3 (6.7)
Actynomices	0 (0)	0 (0)	3 (6.7)
Other	3 (9.1)	2 (22.2)	5 (11.1)

IV Treatment n (%)	Ear	Nose	Deep neck
AC	24 (72.7)	7 (77.8)	36 (80)
AC + metronidazole	2 (6.1)	0 (0)	4 (8.9)
CC	2 (6.1)	1 (11.1)	0 (0)
Ampicillin	3 (9.1)	0 (0)	1 (2.2)
Cefotaxime	2 (6.1)	1 (11.1)	0 (0)
VCM	0 (0)	0 (0)	2 (4.4)
Vancomycin	0 (0)	0 (0)	1 (1.1)
AC + clindamycin	0 (0)	0 (0)	1 (1.1)

AC: Amoxicillin-clavulanic acid. CC = Cefotaxime + clindamycin. VCM = Vancomycin + ceftriaxone + metronidazole.

Regarding surgical treatment, the most common interventions of each area were as follows: transoral drainage for neck infections (48.3%), myringotomy ± tube insertion regarding ear infections (31%) and endoscopic sinus surgery ± external approach in case of complicated nasal infections (2.3%).

The overall mean of time of hospitalization was 3.79 (±3.5) days, requiring intensive care surveillance only 4 out of 87 patients. Afterwards, patients were discharged receiving an oral antibiotic until completing 12.93 (±6) days of treatment. Amoxicillin- clavulanic acid was the preferred oral treatment (82.8% of children). However, a change in trend was noticed in the 3^rd period, with a statistically increase in the use of Amoxicillin (p = 0.047) and a subsequently decrease of Amoxicillin-clavulanic acid (p = 0.028).

Evolution (Table 4)

4 patients (4.6%) were readmitted in the hospital because of a bad evolution of the infection. All of them were primarily diagnosed of acute mastoiditis, treated with Amoxicillin-clavulanic acid plus ear tube insertion. Subsequently, drill mastoid surgery was performed in all of them with a final good evolution.

Only one patient (1.1%) experienced a complication during his hospitalization stay. He had been treated for his peritonsillar abscess with transoral drainage and amoxicillin-clavulanic acid. After appearance of Fusibacterium in the culture, Metronidazole was added. However, due to bad evolution, CT was performed which confirmed internal yugular vein thrombophlebitis with cervical and pulmonary abcesses (Lemierre Syndrome). Subsequently, anticoagulants were administered and he prolonged his hospital stay for 17 days. Moreover, a year after the episode, tonsillectomy was performed.

Discussion

In our experience, ENT infections pattern has changed after pandemic. Therefore, the principal purpose of our project is to investigate if there is a real change in the upper respiratory tract infection profile in Madrid after COVID-19 pandemic. Specifically, we intend to discover whether there is a shift in microorganisms involved and treatment performed. With this purpose, Pubmed database was searched. Despite there are multiple reports focused on repercussion of COVID-19 and ENT infections during pandemic, still little bibliography is published approaching post-pandemic consequences. In fact, we only found a similar study developed by Galli et al.⁶ in a tertiary hospital in Switzerland. Interestingly, we obtained very similar results, what make us think about a worldwide change in ENT infectious pattern after COVID-19 pandemic.

Historically, ENT infections in children had been relatively stable over time, showing a peak during winter months and reducing its rate during summer. This effect is called the winter effect and it is mainly explained because of changes in environmental temperature and humidity and its influence in human immunity.⁷ However, we have observed a change in trend after declaration of COVID-19 pandemic. As proved before, we have seen a decrease in ENT complications during the pandemic followed by a raise after relaxation of preventive measures. Moreover, no more predominance of winter season is observed after pandemic (Fig. 1). This fact might be explained because preventive measures established for COVID-19 prevented as well for other upper tract infections. As a result, there is lack in development of immunity for common pathogens. Hence, after pandemic, this immunity debt provokes a catch-up effect from previously prevented infections and an increase in ENT infections is seen.⁸ Nevertheless, similar to Galli et al.⁶ report, we have only obtained a significant result regarding ear infections (p = 0.033).

We have also observed a change in microorganism pattern regarding pandemic period (Fig. 2). In the past, Fusobacterium role in upper respiratory tract infections was minority. However, a remarkable increase in the past ten years had been observed specially in deep neck infections,^4,5 and less frequent in ear infections.⁹ Regarding Streptococcus pyogenes, its involvement in ENT infections remained stable over time, until December 2022, when the UK government alerted of an unusual increase in invasive infections caused by Group A Streptococcus.^10–12 Subsequently, several countries have reported a similar rise in both the number and severity of Steptococcus pyogenes infections. In Spain, determining the exact incidence is particularly challenging, as it is not a notifiable disease. However, a study conducted by the Pediatric Infectology Group of the Spanish Pediatric Society indicates that there has also been a significant increase in cases, doubling the incidence rate in 2023 compared to 2022. Despite this, it appears that the circulating strains are similar to those of previous years, with predominance of M1 serotype and do not show increased resistance to standard antibiotics (Penicillin or Clindamycin). Therefore, in their review, they attribute this increase to the immunological deficiency left by the pandemic in children due to the lack of infectious stimuli, highlighting the need for further studies to assess long-term effects in the coming years. In our cohort, we obtain similar results, with a remarkable predominance of Fusobacterium species (p = 0.001) during COVID-19 pandemic at the expense of deep neck infections and a subsequent change in trend towards Streptococcus (p = 0.049) and, more precisely, Streptococcus pyogenes (p = 0.028) after abolishment of preventive measures causing ear complications.

Figure 2.

Change in trend of pathogens regarding pandemic period.

Lastly, due to pathogen trend shift, we have observed a change in antibiotic therapy. According to clinical guidelines,¹³ Fusobacterium might be treated with a beta-lactam such as Amoxicillin-clavulanic acid, Ceftriaxone or Meropenem usually combined with Metronidazole. Nevertheless, if appearance of Lemierre’s syndrome as a complication, prognosis worsens and a more aggressive treatment should be applied, including anticoagulants and prolongation of antibiotic treatment up to 6 weeks.

Regarding Streptococcus pyogenes, guidelines^4,5 suggest using Penicillin or Amoxicillin. In our sample, we see a greater proportion of Amoxicillin-clavulanic acid oral usage in 1^st and 2^nd period (p = 0.028) probably associated with the need of covering anaerobic bacteria such as Fusobacterium. Moreover, we do see an increase in oral administration of Amoxicillin after pandemic (p = 0.047), which would be enough for covering Streptococcus pyogenes. It is not observed a statistical association between intravenous Amoxicillin-clavulanic acid and the analyzed period although a decrease in proportion is seen (1^st: 96.3%, 2^nd: 85.7%, 3^rd: 73.9%). This might be explained because in our center Amoxicillin-clavulanic acid is the choice empirical treatment for most ENT infections. Therefore, it is usually administered for some days until microbiology report is given and then, treatment is deescalated to an oral, reduced-spectrum antibiotic.

Conclusions

COVID-19 pandemic has changed the profile of ENT infections in our area of influence in Madrid, Spain. Following the abolition of social prevention measures, we have experienced a statistical increase in ear infections, primarily caused by Group A Streptococcus, leading to a rise in urgent surgical interventions. These results are similar to those reported in other parts of the world. Therefore, this paper pretends to highlight the importance of the updated ENT pediatric infection profile, encouraging physicians to adapt the treatment strategy.

Limitations

However, our study has few limitations. Firstly, it is a retrospective analysis so, even though we have included all surgical records, a selection bias might be present and could limit our findings. Secondly, our study was conducted in a single hospital and, despite we cover a big population area in Madrid, our results might not be applicable for other regions or countries. Thirdly, we have not included those children who had an ENT infection but did not need a surgical intervention and these would have been interesting to compare differences in medical management in both groups.

Lastly, since there is little published literature on the subject, we have not yet found a justification for the statistically significant selective increase in ear infections but not in cervical or nasal infections. Further studies are necessary to be able to formulate a hypothesis.

It would be interesting for the future another multicentric study involving referral hospitals from different countries in order to provide more strong evidence.

CRediT authorship contribution statement

MAD, MAAR and MHC designed the work; ALB, JAPP, CMO,MST and RSE acquired and analysed data; MAD, MHC and MMAR drafted, revised and approved the manuscript; MAD agree to be accountable for all aspects of the work.

Ethical considerations

This research was conducted in accordance with the Declaration of Helsinki and was approved by the appropriate institutional review board

Financial disclosures/conflicts of interest

This study received no external funding. The authors declare that there are no financial interests or conflicts of interest related to this research. his research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. (ORLHGUGM_II).

Data availability

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.