Experience of flexible bronchoscopy in the pediatric pulmonary diseases clinic

ABSTRACT Experience of flexible bronchoscopy in the pediatric pulmonary diseases clinic Introduction: Flexible bronchoscopy is a valuable method in the diagnosis and treatment of respiratory tract diseases in children. This study aimed to examine the indications for and results of flexible bronchoscopy in children. Materials and Methods: The study included patients aged 0-18 years who underwent flexible bronchoscopy between 1 January 2017 and 31 December 2022. The patients were evaluated for demographic characteristics, indica- tions for bronchoscopy, comorbidities, bronchoscopy findings, and the results of bronchoalveolar lavage. Results: During the defined study period, a total of 410 flexible bronchoscopy procedures were performed. 51.9% of the patient population were male, and 48.1% were female, with a mean age of 96.93 ± 63.45 months. The most common indication for flexible bronchoscopy was recurrent lower respiratory tract infection (26.8%), followed by chronic cough (19.1%). The bronchoal- veolar lavage culture results showed that the most commonly isolated micro- organisms were H. influenzae non-type b (7.8%) followed by M. catarrhalis (7.3%). Mucus obstruction and secretion (33.0%) constituted the most com- mon bronchoscopic findings, while the flexible bronchoscopy examination was normal in 27% of patients. No serious complications occurred in any patient during or after the procedure. Conclusion: The results of this study demonstrated that the most common indication for flexible bronchoscopy was recurrent lower respiratory tract infection and the most common bronchoscopy finding was purulent secretion with mucus obstruction. Flexible bronchoscopy is an important diagnostic and treatment tool for patients with recurrent respiratory symptoms. It is a highly valuable method as it enables direct visualization of the airways and facilitates the collection of bronchoalveolar lavage samples. Key words: Flexible bronchoscopy; bronchoalveolar lavage ÖZ Çocuk göğüs hastalığı kliniğimizde fleksible bronkoskopi deneyimlerimiz Giriş: Fleksible bronkoskopi çocuklarda solunum yolu hastalıklarının tanı ve tedavisinde kullanılan değerli bir yöntemdir. Bu çalışmada amacımız çocuklar- da fleksible bronkoskopi endikasyonlarını ve sonuçlarını araştırmaktır. Materyal ve Metod: Çalışmaya çocuk göğüs hastalıkları bilim dalımızda 1 Ocak 2017 ile 31 Aralık 2022 tarihleri arasında 0-18 yaş arasında fleksible bronkoskopi yapılan hastalar dahil edildi. Hastaların demografik özellikleri, bronkoskopi yapılma endikasyonu, eşlik eden komorbiditeler, bronkoskopi bulguları ve bronkoalveolar lavaj sonucu kaydedildi. Bulgular: Toplam 410 FB işlemi uygulanmıştı. Hastaların %51,9’u erkek, ortalama yaşları 96,93 ± 63,45 aydı. Fleksible bronkoskopi- nin en sık endikasyonu tekrarlayan alt solunum yolu enfeksiyonu (%26,8), ikinci en sık endikasyon kronik öksürük (%19,1) idi. Bronkoalveolar lavaj kültür sonucu en sık üreyen mikroorganizma H. influenzae non-tip b (%7,8) iken ikinci sıklıkla M. catarrhalis (%7,3) idi. En sık bronkoskopik tanı mukus tıkacı ve sekresyon (%33,0) iken, hastaların %29,7’sinin fleksible bronkoskopisi normal- di. İşlem esnasında ve sonrasında ciddi bir komplikasyon gelişen hasta olmadı. Sonuç: Çalışmamızda en sık FB endikasyonu tekrarlayan alt solunum yolu enfeksiyonu iken en sık bronkoskopi bulgusu pürülan sekresyon ve mukus tıkacıydı. Fleksible bronkoskopi, tekrarlayan solunum semptomları olan hastalarda önemli bir tanı ve tedavi ara- cıdır. Hava yollarının direk görüntülenebilmesi ve bronkoalveolar lavaj örneğinin alınabilmesi ile çok değerli bir yöntemdir. Anahtar kelimeler: Fleksible bronkoskopi; bronkoalveolar lavaj


INTRODUCTION
Flexible bronchoscopy (FB), which is widely used in the diagnosis and treatment of respiratory tract diseases, provides the opportunity to visualize upper and lower airways, thereby allowing anatomic and dynamic information about the airways to be obtained (1).The main aim of pediatric flexible bronchoscopy continues to be diagnostic (2).The diagnostic indications include stridor, chronic cough, recurrent wheezing, recurrent lower respiratory tract infections, structural anomalies, hemoptysis, and radiological anomalies (2,3).As a result of the evaluation of the upper respiratory tract, functional and structural airway anomalies such as choanal atresia, subglottic stenosis, laryngeal cyst, and vocal cord dysfunction can be diagnosed with FB (3).However, in children, this procedure requires deep sedation (3).
Samples for diagnostic purposes can be obtained by advancing as far as the distal ends of the lungs with the bronchoalveolar lavage procedure.Saline, which is soluble in alveolar fluid is administered to the distal airways and then withdrawn.The cell ratios on the alveolar surface can be measured in the fluid, and cytological and microbiological studies can be performed (4)(5)(6).Microbiological tests of cultures, polymerase chain reaction (PCR), and cell count analysis can be made.For diagnostic purposes, hemosiderin-loaded macrophages, lipid-loaded macrophages, and immunological tests can be performed.
For both diagnosis and treatment, bronchoscopy is important in immunocompromised patients (7).Appropriate samples can be obtained from cystic fibrosis patients, which can guide antibiotic treatment (7,8).Whole lung lavage is another method of obtaining samples from the lungs and is used in pulmonary alveolar proteinosis treatment.Although rigid bronchoscopy is accepted as the gold standard for the removal of foreign bodies, flexible bronchoscopy can also be used (9).
Usually, no complications are seen after the procedure, and the most common airway complications that may be encountered are laryngospasm and rupture.Therefore, patients must be closely monitored and oxygen support should be given.
This study aimed to investigate the indications for flexible bronchoscopy performed in our center and to examine the bronchoscopy results.

MATERIALS and METHODS
Approval for this retrospective study was granted by the Ethics Committee of the Medical Faculty (decision no: 23-11T/37).Written consent was obtained from all patients and their parents.The study included patients aged 0-18 years who underwent flexible bronchoscopy between January 2017 and December 2022.The demographic characteristics, indications for bronchoscopy, bronchoalveolar lavage fluid culture results, comorbidities, and bronchoscopy findings were recorded for all the patients.The bronchoscopy procedure was performed using a 2.8 mm diameter bronchoscope for infants and young children (BF-XP160F Evis Exera, Olympus, Japan) and a 3.2 mm diameter bronchoscope for older children (BF-3C Evis Exera, Olympus, Japan).Written informed consent was provided by the parents of all the children before the procedure.The bronchoscopy procedure was performed in the operating theatre after patients fasted for six hours.Airway safety was ensured using either a laryngeal mask or an endotracheal tube, depending on the patient's clinical status.The bronchoalveolar lavage procedure was performed by instilling 1 mL/kg of Anahtar kelimeler: Fleksible bronkoskopi; bronkoalveolar lavaj saline three times for patients weighing <20 kg, and with 20 mL of saline for patients weighing >20 kg.
All FB procedures were performed by a senior specialist in pediatric chest diseases.The bronchoalveolar lavage (BAL) samples were taken from the right middle lobe and the left lingular segment (9,10).In patients with localized atelectasis and findings of infection, samples were taken from the lobes where the findings were detected radiologically.The diagnosis of airway malacia was made from visual examination during the bronchoscopy in spontaneous respiration (11,12).The bronchoscopy secretion type was classified as type 1, type 2, or type 3 secretion.Type 1 is defined as no secretion in less than a third of all the bronchi, type 2 as secretions filling between one-third and two-thirds of all the bronchi, and type 3 as secretions filling more than two-thirds of all the bronchi.According to the bronchoscopic secretion score, six grades were defined; grade 1: no secretion, grade 2: bubbles in less than half of the bronchi, grade 3: type 1 secretion in less than half of the bronchi, grade 4: type 1 secretion in more than half of the bronchi or type 2 secretion in less than half of the bronchi, grade 5: type 2 secretion in more than half of the bronchi, grade 6: type 3 secretion in less than half of the bronchi.Throughout the procedure, the heart rate, blood pressure, and oxygen saturation rates of all the patients were continuously monitored.
As this was a retrospective study, patients with incomplete information in the files were excluded from the study.

Statistical Analysis
Statistical analysis was performed using SPSS software (version 23.0;IBM SPSS Statistics).Values are expressed as mean ± standard deviation for continuous variables, median and range for nonparametric data, and number and percentage (%) for categorical variables.
FB was performed on 78 patients due to chronic cough, and the results were normal in 41% of these patients.Persistent bacterial bronchitis was determined in 12 (15.4%)patients, anatomic defect in 10 (12.8%), and foreign body aspiration in four.The most commonly identified pathogen in the bronchoalveolar lavage fluid of patients with chronic cough was M. catarrhalis.
FB was performed on 25 patients due to immune deficiency.The most common findings on the radiological imaging of these patients were peribronchial thickening, ground-glass appearance, hilar-mediastinal lymphadenopathy, and atelectasis.
The most commonly identified pathogen in the bronchoalveolar lavage fluid of these patients was S. aureus (62.1%).When the bronchoalveolar lavage results were examined, there was no growth in the cultures of 56.6% of the patients.The three most commonly isolated microorganisms were H. influenzae non-type b (n= 32, 7.8%), M. catarrhalis (n= 30, 7.3%), and S. pyogenes (n= 26, 6.3%).The bronchoalveolar lavage culture results are shown in Table 3.In one patient with a recurrent lung infection, P. aeruginosa was isolated in the BAL fluid, and as the sweat test indicated high levels, the patient was referred for genetic analysis and subsequently diagnosed with cystic fibrosis.
Of the 22 patients who underwent FB due to suspected foreign body aspiration, a foreign body was determined in 11 (50%) patients.These foreign bodies were dried fruit/nuts in seven patients, a piece of a toy in two, part of a pen in one, and paper packaging in one.These were all removed with rigid bronchoscopy by a pediatric surgeon.
No major complications were observed in any patient during or after the procedure.During the procedure, there was a drop in oxygen saturation in 15 (3.6%) patients.In three of these cases, the procedure was terminated, and in 12 the procedure was continued after the oxygen saturation level was restored.

DISCUSSION
There is increasing use of FB in children for diagnostic and treatment purposes.Although FB is an invasive procedure, the complication rate is low.Bronchoalveolar lavage fluid is highly valuable for diagnosis.It is a versatile test as it allows for culture, PCR, pathology, cytology, and immunological tests to be conducted.The use of FB is recommended in recurrent, prolonged conditions such as recurrent lower respiratory tract infections and chronic cough.This study aimed to present the indications for and results of flexible bronchoscopy performed in our center over six years.
The mean age of the patients in this study was 96.93 ± 63.45 months, and the most common indication for FB was recurrent lower respiratory tract infection (26.8%), followed by chronic cough (19.1%).In a previous large-scale study conducted in Türkiye, the mean age of patients was 84 months, and the most common indication for FB was reported to be recurrent pneumonia (17%) (13).Consistent with the current study, a study reported that recurrent respiratory tract infection (32.2%) was the most common indication for bronchoscopy (14).Recurrent respiratory tract infections are among the most common reasons for presentation at the pediatric thoracic diseases outpatient clinic, with various etiological factors contributing to this phenomenon.FB should be performed for diagnostic purposes in cases with recurrent lower respiratory tract infections and etiology that cannot be determined with existing diagnostic methods.
The second most common indication for bronchoscopy in the current study was chronic cough (19.1%).The study reported that 32% of bronchoscopy indications were tracheal, laryngeal, or chronic wet cough (14).A chronic cough is an important finding of respiratory tract diseases in children.The most frequent causes of chronic cough include asthma, post-infection cough, and bronchiectasis.Patients with a suspected diagnosis and for whom the chronic cough cannot be improved with medical treatment should be evaluated with FB.The European Respiratory Society (ERS) guidelines recommend airway bronchoscopy for patients with a persistent chronic wet cough following four weeks of appropriate antibiotic use (15).If non-invasive sampling cannot be achieved in children with lower respiratory tract infections unresponsive to antibiotic treatment, bronchoscopy is recommended (16,17).The isolation of the causative agent in patients with chronic cough guides the selection of antibiotics and treatment.
The laryngeal mask is the most commonly utilized method for ensuring airway safety and has been proven to be effective and safe.The American Thoracic Society has recommended that airways can be better evaluated during spontaneous respiration and the procedure should be continued afterward with a laryngeal mask (LMA).Additionally, the use of LMA is associated with a lower risk of abdominal distension and aspiration.Bronchoscopy can be performed using an endotracheal intubation tube, but it carries a greater risk of hypoxemia and hypercarbia.Especially in critical patients with poor cardiopulmonary reserves, hypoxemia can develop due to decreased tidal volume, intrapulmonary shunt (V/Q incompatibility), and the frequent aspiration and administration of saline for BAL, which washes away the surface active substance and causes alveolar overflow.In the current study, LMA was used in 95.6% of the patients, and a drop in oxygen saturation was seen in 3%, but no major complication developed in any patient.
The most common bronchoscopy finding in the current study was mucus obstruction with purulent secretion.The variability in its determination across different studies could be attributed to the differences in selected patient groups.The bronchoscopy results of the current study can be attributed to the most common bronchoscopy indications being determined as recurrent pneumonia and chronic cough.Mucus obstruction and purulent secretion, commonly associated with chronic disease, can also be indicative of conditions such as foreign body aspiration or poorly treated pneumonia.These presentations may result in radiological evidence of atelectasis, necessitating FB in such cases.
Of the 22 FB procedures performed in this study due to suspected foreign body aspiration (FBA), a foreign body was identified in 50%, all of which were subsequently removed by a pediatric surgeon using rigid bronchoscopy.If there is a history of FBA, even if the physical examination findings are normal, FB should be performed in suspected patients.FBA can cause various clinical conditions ranging from recurrent lung infections to asphyxia and death.The most common symptoms are obstruction, dyspnea, cough, stridor, and cyanosis.Occasionally, subcutaneous emphysema may develop.In 40% of patients, there is no history of FBA.In the physical examination, there may be a decrease in respiratory sounds in the lung where the foreign body has settled, and rales and rhonchus can be heard in other areas.Rigid bronchoscopy continues to be the gold standard in the treatment of FBA in children (18).
The most common comorbidity in this study was immune deficiency.In patients with atelectasis, persistent consolidation on radiological images, and particularly in those with recurrent pneumonia, identifying the causative agent guides medical treatment decisions.Agents that do not grow in standard cultures may grow in BAL fluid.The most common indication in patients with immune deficiency was determined to be lower respiratory tract infection.In a study by Efrati et al., the most common indication for FB in patients with immune deficiency was reported to be neutropenic fever and respiratory problems (19).Various infectious agents may be implicated in patients with immune deficiency, and effectively clearing secretions can be highly beneficial in the clinical management and follow-up of these individuals.
In 43.4% of the bronchoalveolar lavage fluid cultures, microbial growth was observed.The most commonly identified microorganism was H. influenzae non-type b.The growth of microorganisms may be affected by previous antibiotic use, particularly in cases where no growth is observed.A previous study reported that S. aureus and H. influenzae non-type b were the most commonly isolated microorganisms in BAL fluid (20).Microorganisms may exhibit variability from center to center, potentially attributed to differences in antibiotic resistance profiles and duration of antibiotic use.The type of microorganism detected in BAL fluid can vary depending on the patient's comorbidities and the duration of antibiotic use.
When bronchoscopy complications are examined, hypoxemia is the most frequently seen complication.
Although FB is a safe procedure, studies in the literature have reported the most common complications to be hypoxia, bleeding, infection, and pneumothorax (21,22).Fever following bronchoscopy is a temporary complication that may occur and is often seen in children aged <2 years (23).In the current study, fever developed after the procedure in two patients, but resolved within 24 hours.
For the flexible bronchoscope to be used on another patient after one procedure, it must undergo thorough manual disinfection according to appropriate standards, followed by high-level disinfection.The personnel performing the procedure must have completed training and undergo annual proficiency tests.Personal protective equipment must be used during the procedure and when handling the bronchoscope afterward.

Study Limitations
The main limitation of this study was its single-center, retrospective design.Additionally, due to the retrospective nature of the study, patients with incomplete records were excluded from the study.

CONCLUSION
In conclusion, flexible bronchoscopy is a procedure with few complications that can be safely performed in children.It continues to be increasingly utilized for diagnostic purposes in children.In cases with prolonged respiratory tract problems such as recurrent lower respiratory tract infection, chronic cough, persistent atelectasis, and persistent wheezing, the evaluation of the airway with flexible bronchoscopy and obtaining a BAL sample can be extremely beneficial in reaching a diagnosis.FB should be performed in patients with persistent radiological findings and respiratory complaints and in those with chronic diseases such as cystic fibrosis or immune deficiency.The results of this study revealed that the most frequent indication for FB was recurrent lower respiratory tract infection, with the most common bronchoscopic findings being purulent secretion and mucus obstruction, followed by airway malacia.
There is increasing use of FB in the diagnosis and treatment of respiratory tract diseases in children.

Table 1 .
Demographic characteristics of patients

Table 3 .
Bronchoalveolar lavage culture results