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The complimentary role of diagnostic and therapeutic endoscopy in foreign body aspiration in children
International Journal of Pediatric Otorhinolaryngology 75 (2011) 1481–1485
Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Review article
The complimentary role of diagnostic and therapeutic endoscopy in foreign body aspiration in children Cesare Cutrone a,*, Barbara Pedruzzi a, Giulia Tava a, Enzo Emanuelli b, Umberto Barion b, Daniele Fischetto a, Marianna Sari a, Surendra Narne a, Nicola Zadra c, Alessandro Martini a a
Department of Endoscopic Airways Surgery, Azienda Ospedaliera di Padova, Via Giustiniani 1, Padova, Italy1 Department of Otorhinolaryngology-Otosurgery, Azienda Ospedaliera di Padova, Padova, Italy c Department of Pediatric Anesthesia, Azienda Ospedaliera di Padova, Padova, Italy
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 May 2011 Received in revised form 17 August 2011 Accepted 19 August 2011 Available online 15 September 2011
Objective: To review the importance and benefits of flexible bronchoscopy and rigid bronchoscopy in airway foreign body inhalation in children. Prompt diagnosis will lead to safer outcomes when both types of endoscopy are employed within the operating room setting. Methods: Retrospective review of all cases of foreign body inhalation seen and treated in our Department between July 1986 and December 2010. Results: Three-hundred and ten children were admitted to our Department from Pediatric Emergency Room for a suspected foreign body inhalation. All patients with suspected FB inhalation underwent bronchoscopy. Of 310 evaluations of tracheobronchial tree performed at our Department, 104 were negative, while an airway FB were observed and removed in 206 cases. Conclusions: Rigid bronchoscopy under general anesthesia is an extremely accurate surgical technique to identify, localize and remove airway foreign body. In our experience, flexible bronchoscopy under total intravenous sedation and topical anesthesia is very useful in doubtful cases to absolutely exclude the presence of foreign body in upper airway tracheobronchial tree. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Airway foreign body Foreign body inhalation Rigid bronchoscopy Flexible bronchoscopy
Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . Materials and methods Results . . . . . . . . . . . . . Discussion . . . . . . . . . . Conclusions . . . . . . . . . References . . . . . . . . . .
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1. Introduction Airway foreign body (FB) inhalation in children, although uncommon, is a very dangerous and potentially life-threatening event that requires prompt diagnosis and definitive successful treatment. It is considered a true emergency in the pediatric age group [1]. FB aspiration/inhalation is the most common cause of accidental death in children under 1 year old [2], and the risk for FB aspiration is very high up to 3 years of age [3]. In USA, FB inhalation represents * Corresponding author. Tel.: +39 0498213105; fax: +39 0498213106. E-mail address: [email protected] (C. Cutrone). 1 [email protected]. 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.08.014
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about 7% of deaths in children younger than 4 years of age [4,5]. In Italy, about 400 pediatric FB aspirations occur every year [4]. Many retrospective studies on pediatric FB inhalation have been published in English literature [4–6], and suggested that approximately 80% of pediatric FB inhalation occurs in children under 3 years of age. At this age children tend to explore their environment via the oral route [7] and often they have access to small objects and inappropriate food. Reilly et al. [8] concluded that children 4 years are more susceptible to FB injuries due to their lack of molar teeth, oral exploration of the objects, and poor swallowing coordination. The more frequent inhaled FB are organic items (food, such as peanuts, seeds, and dried fruits) and inorganic items (such as little toys, pen caps and pieces of plastic) [3,6,9]. Organic items are most commonly aspirated in the younger age groups, while older
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children are more likely to inhale inorganic items [6]. The range of aspired FB varies from country to country, depending on diet and customs of the population [10]. The anatomical sites of inhaled foreign bodies are variable. Due to the anatomic and physiological characteristics of airways, most FB are located in the right bronchial tree [4,11]. In the majority of cases, the FB tends to lodge distally, in one of the main bronchi or its branches, in which case the clinical condition is likely to be more stable [6]. FB inhalation must be suspected from a witnessed choking episode. History of an inhalation event is elicited in 80% of cases [6]. Signs and symptoms associated with FB inhalation are observed in 3 stages [12]. Initially, there is chocking episode followed by violent coughing, gagging, and possibly complete airway obstruction. An asymptomatic period follow: the FB is lodged and reflexes become fatigued, resulting in the symptoms died down. The third stage is characterized by symptoms of complications. Children who present with signs of severe respiratory distress require urgent rigid bronchoscopic removal of the foreign body. However, more commonly the clinical situation is relatively stable, and often signs and symptoms are nonspecific [13]. In these cases clinical examination may reveal cough, wheeze and focally reduced air entry on chest auscultation [6]. Parents or caregivers may not witness or remember chocking episodes, and children may not disclose a history of chocking or of inhaling FB [7]. Children often are unable to communicate the circumstances leading to the aspiration event [13], because of limited speech, fear of being punished or embarrassment [14]. Various series have shown presentation within 24 h of inhalation to occur in between 50 and 75% of cases [6]. Diagnosis of an inhaled FB was delayed by more than a week in 29% of cases and by more than 30 days in 10% [15]. If misdiagnosed, it may cause chronic and irreversible lung injury [13]. Inhaled FB that do not cause an intense inflammatory response (i.e. piece of plastic) or that result in only partial airway occlusion are the most difficult to detect [7]. The rate of serious complications (including pneumonia, atelectasis, bronchiectasis, pneumothorax, and subglottic oedema) is 2.5 times higher when diagnosed more than 24 h after aspiration, than when diagnosed within 24 h [7]. Long term complications (such as chronic persistent cough, recurrent pneumonia, lung abscess, and bronchiectasis) rates are higher if diagnosis is delayed [7]. The decision to perform bronchoscopy is based on history, physical examination, and radiologic findings. However no single parameter of diagnostic tools (history, auscultation, and chest Xray) is both sensitive and specific for diagnosis [16], and positive findings usually are not specific to FB inhalation, and may occur in condition mimicking FB inhalation or may be absent in some cases [5]. Airway FB aspiration continues to be a diagnostic and therapeutic challenge for otolaryngologists and pediatricians [17]. Definitive diagnosis of FB aspiration is by endoscopic evaluation. In children with higher suspected FB inhalation (such as suggestive history, symptoms, signs, or chest radiograph findings), rigid bronchoscopy under general anesthesia is indicated. Rigid bronchoscopy was the procedure of choice for the diagnosis and treatment of FB inhalation in pediatric patients [4,7]. In cases where clinical and radiographic findings are equivocal, flexible bronchoscopy under total intravenous sedation and topical anesthesia is very useful in confirming the presence and the exact site of FB [7]. The most appropriate procedure depends on the likelihood of FB being present, but is always performed in the safety of the operating room. 2. Materials and methods From July 1986 to December 2010, 310 children were admitted to Department of Endoscopic Airways Surgery of Padua Hospital
(Italy) from Pediatric Emergency Room for a suspected FB inhalation. They all have a history of suspected FB inhalation. Each patient was examined by an experienced team of pediatricians and/or otolaryngologist, that evaluated the history, symptomatology, physical examination (especially objective chest evaluation) and radiologic findings. Written informed consents to perform bronchoscopy and anesthesia were given by parents or legal tutors before the procedure and then all of them underwent bronchoscopy within 24 h of hospitalization. Flexible or rigid bronchoscopy was performed after 6 h of fasting, under general anesthesia or under sedation and topical anesthesia. All bronchoscopies were performed by qualified pediatric otolaryngologist, in close cooperation with an experienced anesthetist. The surgical procedures were always performed in operative room, where patients were continuously monitored for heart rate, electrocardiography, pulse oximetry and non-invasive blood pressure at 5 min intervals. When identified, the FB was removed using rigid broncoscopes equipped with optic telescopes and camera. The size and the length of instruments were related to the age and weight of each child. Alligator or peanut-type forceps were used to grasp the FB. During endoscopic procedures, all children were in controlled respiration or positive pressure ventilation with high FiO2 and breathed with high rates of oxygen through a circuit connected to the rigid bronchoscope. Total intravenous anesthesia (TIVA) was used for the induction and maintenance of anesthesia in all patients, associated with topical airway anesthesia with lidocaine 2%. All patients with suspected FB inhalation underwent bronchoscopy. From July 1986 to December 2008, only rigid bronchoscopies under general anesthesia were performed. From January 2009 to December 2010, in doubtful cases a flexible bronchoscopy under total intravenous sedation and topical anesthesia was performed to identify the presence of FB and its exact site. During the procedure, the rigid bronchoscopy was anyway ready for use. If negative the endoscopy stopped. If positive, the patient promptly underwent rigid bronchoscopy under general anesthesia to remove the FB. After the removal of the FB, the tracheobronchial tree was investigated for a second time to detect others retained fragments or to look for iatrogenic injury. During the procedure, a dose of intravenous corticosteroids (i.e. betamethasone 0.1 mg/kg die) was always administered. A postoperative aerosol with corticosteroids was done in each patients. If no complications occur, the patients were dismissed the day after the procedure. 3. Results From July 1986 to December 2010, 310 children were admitted to Department of Endoscopic Airways Surgery of Padua Hospital (Italy) from Pediatric Emergency Room for a suspected FB inhalation. One hundred and eighty-four (59.4%) were male and 126 (40.6%) female. The children have an age from 1 month to 14 years (mean age: 2.7 years; median age: 1.6 years). Two hundred and forty-six of the 310 patients (79.4%) were under 3 years of age, while the remaining 64 (20.6%) were older than 3 years. A witnessed inhalation was described in 274 (88.4%) children. All 310 patients were so classified: children with abnormal physical and radiologic findings with symptoms (108 cases), children with abnormal physical findings and normal radiologic findings with symptoms (86 cases), children with normal physical findings and abnormal radiologic findings without symptoms (10 cases), children with normal physical and radiologic findings but with symptoms (74 cases), and children with normal physical and radiologic findings and without symptoms (32 cases).
C. Cutrone et al. / International Journal of Pediatric Otorhinolaryngology 75 (2011) 1481–1485
Two-hundred and thirty-six (76.2%) patients were referred to our Department within the first 24 h of the event, while 74 (23.8%) patients were admitted and evaluated many hours later. All patients with suspected FB inhalation underwent bronchoscopy. From July 1986 to December 2008, only rigid bronchoscopies under general anesthesia were performed. From January 2009 to December 2010, a flexible bronchoscopy under sedation and topical anesthesia was performed to identify the presence of FB and its exact site. If negative the endoscopy stopped. If positive, the patient underwent rigid bronchoscopy under general anesthesia to remove the FB. So, from January 2009 to December 2010, 30 patients (9.7%) underwent flexible endoscopy to investigate the tracheobronchial tree. Twelve cases of 30 (40%) were negative, stopping the operation and saving the risk of rigid bronchoscopy under general anesthesia. Of 310 evaluations of tracheobronchial tree performed at our department, 104 (33.5%) were negative, while an airway FB were observed and removed in 206 cases (66.5%). Positive cases were male in 123 (59.7%) and female in 83 (40.3%). Most FB were organic in nature in 185 cases (89.8%): 84 (45.4%) peanuts, 23 (12.4%) almonds, 19 (10.3%) walnuts, 10 (5.4%) raw carrots, 6 (3.2%) organic undefined materials, 5 (2.8%) hazelnuts, 5 (2.8%) vegetable fragments, 4 (2.2%) piece of chicken bones, 4 (2.2%) chestnuts, 4 (2.2%) pistachio, 3 (1.6%) food, 2 (1.1%) pieces of apple, 2 (1.1%) maize seeds, 2 (1.1%) sugared almonds, 2 (1.1%) meat fragments, 2 (1.1%) dried fruits, 1 (0.5%) bean seed, 1 (0.5%) piece of fennel, 1 (0.5%) chickpea, 1 (0.5%) lupin, 1 (0.5%) pop corn, 1 (0.5%) seed, 1 (0.5%) pumpkin seed, and 1 (0.5%) orange stem. Inorganic FB were found in 21 patients (10.2%): 8 (38.6%) pieces of plastic, 2 (9.5%) pins, 2 (9.5%) metallic undefined objects, 2 (9.5%) pieces of pen, 1 (4.7%) earring, 1 (4.7%) led, 1 (4.7%) metallic screw, 1 (4.7%) wood fragment, 1 (4.7%) piece of cork, 1 (4.7%) metallic bilia, and 1 (4.7%) rub fragment. In 98 cases of the 206 (47.6%) the FB were located in the right bronchial tree, in 82 (39.8%) in the left bronchial tree, in 13 (6.3%) in trachea, in 5 (2.4%) in larynx (hypoglottic cone), and in 1 case (0.5%) it was wedged in lung. FB of 7 patients (3.4%) was bilateral and was removed from both of the bronchi. In the case of the inhaled FB wedged in lung (it was a pin), rigid bronchoscopy was helpful to localize the FB, but it was impossible to remove the pin with this procedure because it was lodge too peripherally, and the extraction was done by thoracic surgeon with a thoracotomic approach. There were not postoperative major complications. Only reasonable bleeding in 6 patients (2.9%) with sharp or pointed metallic FB lodged or wedged in bronchial mucosa. The bleeding stopped with diluted adrenaline administrated by aerosol. Our complications (such as slight dyspnea or mild laryngeal oedema) were transient and resolved without sequelae with the corticosteroids administered (intravenously and by aerosol).
4. Discussion According to literature, our data showed a prevalence in male [5,9,17,18] younger than 3 years [5,6,12,19], and these may be associated with more activity involved in boys, and the function of protection of epiglottis that is not good/mature in childhood [13]. There are also many others speculations regarding the pathophysiology of FB inhalation: lack of molars necessary for proper grinding of food, tendency of children to explore the environment by placing objects in their oral cavity, inadequate chewing of food, not yet developed neuromuscular mechanisms for swallowing, immaturity of the coordination between swallowing and respiration, and often children play or run or jump or laugh while eating and do not pay attention on chewing and swallowing [12,17].
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According to the literature where the range of finding FB in children with suspected FB aspiration is between 25% and 90% [20], in our study FB were found in 66.5% of the 310 children with a suspected FB inhaled. In addition, according to the literature, most FB inhaled in our data were organic items [9,14,19]. Most frequently, FB were located in the right bronchial tree, probably due to the position of the carina to the left of the midline and its lesser angle of divergence from the tracheal axis [4,17]. A witnessed chocking event is the most important historical information in order to have an early diagnosis of FB inhalation [7]. In literature, it is has been reported to be the most sensitive and specific diagnostic tool and reliable history was noted in 22–86% of patients with suspect of FB aspiration [5]. Paroxysm of coughing and raspy breathing followed by wheezing were the most common presenting symptoms [5]. Other symptoms reported, but uncommon, are tachypnea, nasal flaring, and intercostals and suprasternal retraction [5]. A careful history and physical examination were strong indicators of the diagnosis and raised the index of suspicion of an aspirated FB. Without an adult witness, it can be very difficult to document the acute event, and without confirming history the diagnosis of an FB aspiration may be difficult and may produce any of a variety of symptoms, and the patients may be treated for prolonged periods for asthma, asthmatic bronchitis, bronchiolitis [13], pneumonia, or allergy [12]. Undiagnosed and longstanding retained FB may results in asphyxia, pneumonia, atelectasis, bronchiectasis [9], and lung abscesses [7]. Studies have shown that 50% of patients with an FB inhalation lacked causal history, and 20% of children were misdiagnosed and improperly treated for at last 1 month before the correct diagnosis was made [19]. When FB pass through the trachea in to the bronchi, they may cause partial obstruction of airway and consequent changes in auscultation, including crepitations and wheezes. Unilaterally findings had a higher specificity [16]. Bilaterally findings are less suggestive. Asymmetric decrease in breath sounds and presence of rales were the most frequent findings in patients with FB inhalation, but chest auscultation findings have a poor specificity (26%) [5]. Less common but more specific to FB inhalation is obstructive-induced local hyperinflation or even obstructive emphysema with check-valve mechanism [16]. Symptoms associated to alteration of the vesicular murmur, and the presence of pathological noises upon thoracic auscultation play a fundamental role in planning bronchoscopy [4]. Inhalation of nuts usually determinates more severe signs and symptoms due to local inflammation, oedema, cellular infiltration, ulceration and granular tissue formation that may contribute to airway obstruction [10] and consolidation distal to obstruction. The inflammatory response is much more significant with groundnuts because of their rich in oil [14]. In these cases, bronchoscopic removal is urgent, but it is also difficult identify and remove the organic FB because the airway mucosa becomes more likely to bleed with manipulation [10]. The specificity approached 100% in the presence of witnessed aspiration, chocking, and unilateral decreased breath sounds [14]. Radiography of the airway associated with fluoroscopy can be a useful diagnostic procedure, particularly when it can directly show a FB if is composed of radioopaque material. Moreover sometimes it demonstrate indirect radiological findings of a suspicious FB inhalation such as air trapping, obstructive emphysema, infiltrates and atelectasis, lung hyperinflation, collapse and consolidation, pneumonia, and mediastinal shift [21]. Chest X-ray alone is not sufficient for definitive diagnosis, and radiological evaluation of the airway may not be conclusive [13]. In children with FB in airways, chest radiograph findings are
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frequently normal and can show abnormalities uncharacteristic for FB inhalation [12]. A normal chest radiograph does not exclude a FB and this is seen in nearly two thirds of patients with inhaled FB [11]. In the literature, the most common radiologic finding (60%) is air tripping [5], and normal chest X-ray is present in 18–60% of the patients with FB aspirated. The sensitivity of chest radiograph varied between 60% and 90% in the literature, and had a poor specificity [5]. Although chest X-ray is a quite routine in FB aspiration, it has little value in making the differential diagnosis between FB inhalation and respiratory tract infection [5]. Negative radiography should not preclude bronchoscopy in patients with strongly suggestive history and clinical signs [14]. Since Killian’s first demonstration in 1897 [17], transoral rigid endoscopy has been the gold standard approach to remove airway FB [17]. Many other methods were advocated by some authors, such as balloon-tipped catheters, Foley catheter technique, and flexible fibreoptic endoscopy, but rigid bronchoscopy remains the most widely used technique to remove inhaled FB [12,17]. Flexible bronchoscopy is very helpful in the identification and localization of an airway FB [13]. In clear case of FB inhalation (such as a radioopaque FB, a mediastinal shift, or localized wheezing or decreased lung sounds combined with unilateral atelectasis or hyperinflation [3]) or in case of dyspnea, there is no reason to perform flexible and rigid bronchoscopy, so only the rigid one must be done [20]. Flexible endoscopy is recommended as the appropriate diagnostic tool to eliminate doubt in case of equivocal inhalation (such as doubtful history, with or without doubtful physical examination and negative radiological evaluation) and in case of a first severe asthma attack [22], or acute wheezing [17] or unexplained persistent cough with refractory parenchymal infiltrates, or recurrent pneumonia [20] or other respiratory illness or condition that not respond to appropriate medical management [12]. Only the complete view of tracheobronchial tree can exclude the FB presence. Fibreoptic bronchoscopy showed a diagnostic accuracy rate of 100%, but played a poor therapeutic role [9] and, if positive for FB detection, required a promptly rigid bronchoscopy to remove the tracheobronchial FB. Only in high-qualified centres, as ours (3rd level centre), flexible bronchoscopy with total intravenous sedation and local anesthesia is admitted before the rigid bronchoscopy in order to reduce the risks of a rigid bronchoscopy in those patients with no finding of FB. In our operating room dedicated to endoscopy, the rigid bronchoscopy with a variety of forceps is always present and the surgical team is able to promptly shift from a flexible bronchoscopy into a rigid one in a very short time. A close cooperation between anesthesiologists and otorhinolaryngologists with longstanding experience in pediatric airway emergencies is mandatory to obtain successful results. Furthermore the high experience in airways’ emergencies is essential to not incur possible complications and to reduce the mortality rate of this procedure. Extraction failure and complications are rare [9]. Our complication rate of 2.9% was within the limits stated in literature (2– 22%) [5]. Mani et al. [6] analyzed their 25 years experience and reported that, if child is stable, performing rigid bronchoscopy for suspected FB inhalation during normal working hours preferably on an elective list, under optimal conditions, is safe, does not increase morbidity or mortality and allows optimal conditions for performing the procedure, even if this incurs a delay until the following day. Only if patients are clinically unstable with signs of severe respiratory distress, they go to operative room as an out-ofhours emergency. Prevention is the most critical element in reducing mortality and morbidity [9]. Prevention of aspiration of FB is better than the cure [9]! Public awareness through the mass media should stress
the attention and help prevent FB aspiration [23]. Educational campaigns as a public health measure in some counties have brought down the incidence of FB inhalation and the associated mortality [24,25]. Keeping small objects out of the reach of children and education of older children appears to be the most important way to prevent FB inhalation [26]. Small spherically shaped crunchy food items (such as peanuts, nuts and seeds) are those most likely to cause tracheal obstruction and asphyxia. So, all these foods should be forbidden until the child is able to chew them adequately while sitting. Generally, chewing and swallowing become coordinated around the age of 5 years [9].
5. Conclusions FB aspiration is an uncommon life-threatening event in pediatric patients that can manifest with various symptoms. The patient’s history, symptomatology, and objective chest evaluation are very important for planning bronchoscope. Radiological studies may also add useful information, although cannot exclude FB presence in the airway. A close cooperation between anesthesiologists and otorhinolaryngologists with longstanding experience in pediatric airway emergencies is mandatory to obtain successful results. Rigid bronchoscopy under general anesthesia is an extremely accurate surgical technique to remove FB. In our experience, flexible bronchoscopy under sedation and topical anesthesia is the gold standard to absolutely exclude the presence of FB in tracheobronchial tree in doubtful cases and to correctly identify and localize an airway FB. We agree that prevention must remain the main goal in treating FB inhalation in children. References [1] A. Singh, D. Ghosh, C. Samuel, W. Bhatti, Pediatric foreign body aspiration: how much does our community know? J. Indian Assoc. Pediatr. Surg. 15 (October (4)) (2010) 129–132. [2] B.D. Lifschultz, E.R. Donoghue, Deaths due to foreign body aspiration in children: the continuing hazard of toy balloons, J. Forensic Sci. 41 (2) (1996) 247–251. [3] S. Cohen, A. Avital, S. Godfrey, M. Gross, E. Kerem, C. Springer, Suspected foreign body inhalation in children: what are the indications for bronchoscopy? J. Pediatr. 155 (August (2)) (2009) 276–280. [4] F. Pinzoni, C. Boniotti, S.M. Molinaro, A. Baraldi, M. Berlucchi, Inhaled foreign bodies in pediatric patients: review of personal experience, Int. J. Pediatr. Otorhinolaryngol. 71 (December (12)) (2007) 1897–1903. [5] A.O. Ciftci, M. Bingo¨l-Kolog˘lu, M.E. Senocak, F.C. Tanyel, N. Bu¨yu¨kpamukc¸u, Bronchoscopy for evaluation of foreign body aspiration in children, J. Pediatr. Surg. 38 (August (8)) (2003) 1170–1176. [6] N. Mani, M. Soma, S. Massey, D. Albert, C.M. Bailey, Removal of inhaled foreign bodies – middle of the night or the next morning? Int. J. Pediatr. Otorhinolaryngol. 73 (August (8)) (2009) 1085–1089. [7] K. Wang, A. Harnden, A. Thomson, Easily missed? Foreign body inhalation in children, Clin. Otolaryngol. 35 (December (6)) (2010) 494–495. [8] J.S. Reilly, S.P. Cook, D. Stool, et al., Prevention and management of aerodigestive foreign body injuries in childhood, Pediatr. Clin. North Am. 43 (1996) 1403–1411. [9] D. Passa`li, M. Lauriello, L. Bellussi, G.C. Passali, F.M. Passali, D. Gregori, Foreign body inhalation in children: an update, Acta Otorhinolaryngol. Ital. 30 (February (1)) (2010) 27–32 (Review). [10] A. Chinski, F. Foltran, D. Gregori, D. Passali, L. Bellussi, Foreign bodies causing asphyxiation in children: the experience of the Buenos Aires paediatric ORL clinic, J. Int. Med. Res. 38 (March–April (2)) (2010) 655–660. [11] S. Eren, A.E. Balci, B. Dikici, et al., Foreign body aspiration in children: experience of 1160 cases, Ann. Trop. Paediatr. 23 (2003) 31. [12] I.F. Ozguner, B.I. Buyukyavuz, C. Savas, M.S. Yavuz, H. Okutan, Clinical experience of removing aerodigestive tract foreign bodies with rigid endoscopy in children, Pediatr. Emerg. Care 20 (October (10)) (2004) 671–673. [13] F.L. Tang, M.Z. Chen, Z.L. Du, C.C. Zou, Y.Z. Zhao, Fibrobronchoscopic treatment of foreign body aspiration in children: an experience of 5 years in Hangzhou City, China, J. Pediatr. Surg. 41 (1) (2006) e1–e5. [14] F.T. Orji, J.O. Akpeh, Tracheobronchial foreign body aspiration in children: how reliable are clinical and radiological signs in the diagnosis? Clin. Otolaryngol. 35 (December (6)) (2010) 479–485. [15] N. Saki, S. Nikakhlagh, F. Rahim, H. Abshirini, Foreign body aspirations in infancy: a 20-year experience, Int. J. Med. Sci. 6 (October (6)) (2009) 322–328. [16] G. Kadmon, Y. Stern, E. Bron-Harlev, E. Nahum, E. Battat, T. Schonfeld, Computerized scoring system for the diagnosis of foreign body aspiration in children, Ann. Otol. Rhinol. Laryngol. 117 (November (11)) (2008) 839–843.
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Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Review article
The complimentary role of diagnostic and therapeutic endoscopy in foreign body aspiration in children Cesare Cutrone a,*, Barbara Pedruzzi a, Giulia Tava a, Enzo Emanuelli b, Umberto Barion b, Daniele Fischetto a, Marianna Sari a, Surendra Narne a, Nicola Zadra c, Alessandro Martini a a
Department of Endoscopic Airways Surgery, Azienda Ospedaliera di Padova, Via Giustiniani 1, Padova, Italy1 Department of Otorhinolaryngology-Otosurgery, Azienda Ospedaliera di Padova, Padova, Italy c Department of Pediatric Anesthesia, Azienda Ospedaliera di Padova, Padova, Italy
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 May 2011 Received in revised form 17 August 2011 Accepted 19 August 2011 Available online 15 September 2011
Objective: To review the importance and benefits of flexible bronchoscopy and rigid bronchoscopy in airway foreign body inhalation in children. Prompt diagnosis will lead to safer outcomes when both types of endoscopy are employed within the operating room setting. Methods: Retrospective review of all cases of foreign body inhalation seen and treated in our Department between July 1986 and December 2010. Results: Three-hundred and ten children were admitted to our Department from Pediatric Emergency Room for a suspected foreign body inhalation. All patients with suspected FB inhalation underwent bronchoscopy. Of 310 evaluations of tracheobronchial tree performed at our Department, 104 were negative, while an airway FB were observed and removed in 206 cases. Conclusions: Rigid bronchoscopy under general anesthesia is an extremely accurate surgical technique to identify, localize and remove airway foreign body. In our experience, flexible bronchoscopy under total intravenous sedation and topical anesthesia is very useful in doubtful cases to absolutely exclude the presence of foreign body in upper airway tracheobronchial tree. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Airway foreign body Foreign body inhalation Rigid bronchoscopy Flexible bronchoscopy
Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . Materials and methods Results . . . . . . . . . . . . . Discussion . . . . . . . . . . Conclusions . . . . . . . . . References . . . . . . . . . .
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1. Introduction Airway foreign body (FB) inhalation in children, although uncommon, is a very dangerous and potentially life-threatening event that requires prompt diagnosis and definitive successful treatment. It is considered a true emergency in the pediatric age group [1]. FB aspiration/inhalation is the most common cause of accidental death in children under 1 year old [2], and the risk for FB aspiration is very high up to 3 years of age [3]. In USA, FB inhalation represents * Corresponding author. Tel.: +39 0498213105; fax: +39 0498213106. E-mail address: [email protected] (C. Cutrone). 1 [email protected]. 0165-5876/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2011.08.014
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about 7% of deaths in children younger than 4 years of age [4,5]. In Italy, about 400 pediatric FB aspirations occur every year [4]. Many retrospective studies on pediatric FB inhalation have been published in English literature [4–6], and suggested that approximately 80% of pediatric FB inhalation occurs in children under 3 years of age. At this age children tend to explore their environment via the oral route [7] and often they have access to small objects and inappropriate food. Reilly et al. [8] concluded that children 4 years are more susceptible to FB injuries due to their lack of molar teeth, oral exploration of the objects, and poor swallowing coordination. The more frequent inhaled FB are organic items (food, such as peanuts, seeds, and dried fruits) and inorganic items (such as little toys, pen caps and pieces of plastic) [3,6,9]. Organic items are most commonly aspirated in the younger age groups, while older
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children are more likely to inhale inorganic items [6]. The range of aspired FB varies from country to country, depending on diet and customs of the population [10]. The anatomical sites of inhaled foreign bodies are variable. Due to the anatomic and physiological characteristics of airways, most FB are located in the right bronchial tree [4,11]. In the majority of cases, the FB tends to lodge distally, in one of the main bronchi or its branches, in which case the clinical condition is likely to be more stable [6]. FB inhalation must be suspected from a witnessed choking episode. History of an inhalation event is elicited in 80% of cases [6]. Signs and symptoms associated with FB inhalation are observed in 3 stages [12]. Initially, there is chocking episode followed by violent coughing, gagging, and possibly complete airway obstruction. An asymptomatic period follow: the FB is lodged and reflexes become fatigued, resulting in the symptoms died down. The third stage is characterized by symptoms of complications. Children who present with signs of severe respiratory distress require urgent rigid bronchoscopic removal of the foreign body. However, more commonly the clinical situation is relatively stable, and often signs and symptoms are nonspecific [13]. In these cases clinical examination may reveal cough, wheeze and focally reduced air entry on chest auscultation [6]. Parents or caregivers may not witness or remember chocking episodes, and children may not disclose a history of chocking or of inhaling FB [7]. Children often are unable to communicate the circumstances leading to the aspiration event [13], because of limited speech, fear of being punished or embarrassment [14]. Various series have shown presentation within 24 h of inhalation to occur in between 50 and 75% of cases [6]. Diagnosis of an inhaled FB was delayed by more than a week in 29% of cases and by more than 30 days in 10% [15]. If misdiagnosed, it may cause chronic and irreversible lung injury [13]. Inhaled FB that do not cause an intense inflammatory response (i.e. piece of plastic) or that result in only partial airway occlusion are the most difficult to detect [7]. The rate of serious complications (including pneumonia, atelectasis, bronchiectasis, pneumothorax, and subglottic oedema) is 2.5 times higher when diagnosed more than 24 h after aspiration, than when diagnosed within 24 h [7]. Long term complications (such as chronic persistent cough, recurrent pneumonia, lung abscess, and bronchiectasis) rates are higher if diagnosis is delayed [7]. The decision to perform bronchoscopy is based on history, physical examination, and radiologic findings. However no single parameter of diagnostic tools (history, auscultation, and chest Xray) is both sensitive and specific for diagnosis [16], and positive findings usually are not specific to FB inhalation, and may occur in condition mimicking FB inhalation or may be absent in some cases [5]. Airway FB aspiration continues to be a diagnostic and therapeutic challenge for otolaryngologists and pediatricians [17]. Definitive diagnosis of FB aspiration is by endoscopic evaluation. In children with higher suspected FB inhalation (such as suggestive history, symptoms, signs, or chest radiograph findings), rigid bronchoscopy under general anesthesia is indicated. Rigid bronchoscopy was the procedure of choice for the diagnosis and treatment of FB inhalation in pediatric patients [4,7]. In cases where clinical and radiographic findings are equivocal, flexible bronchoscopy under total intravenous sedation and topical anesthesia is very useful in confirming the presence and the exact site of FB [7]. The most appropriate procedure depends on the likelihood of FB being present, but is always performed in the safety of the operating room. 2. Materials and methods From July 1986 to December 2010, 310 children were admitted to Department of Endoscopic Airways Surgery of Padua Hospital
(Italy) from Pediatric Emergency Room for a suspected FB inhalation. They all have a history of suspected FB inhalation. Each patient was examined by an experienced team of pediatricians and/or otolaryngologist, that evaluated the history, symptomatology, physical examination (especially objective chest evaluation) and radiologic findings. Written informed consents to perform bronchoscopy and anesthesia were given by parents or legal tutors before the procedure and then all of them underwent bronchoscopy within 24 h of hospitalization. Flexible or rigid bronchoscopy was performed after 6 h of fasting, under general anesthesia or under sedation and topical anesthesia. All bronchoscopies were performed by qualified pediatric otolaryngologist, in close cooperation with an experienced anesthetist. The surgical procedures were always performed in operative room, where patients were continuously monitored for heart rate, electrocardiography, pulse oximetry and non-invasive blood pressure at 5 min intervals. When identified, the FB was removed using rigid broncoscopes equipped with optic telescopes and camera. The size and the length of instruments were related to the age and weight of each child. Alligator or peanut-type forceps were used to grasp the FB. During endoscopic procedures, all children were in controlled respiration or positive pressure ventilation with high FiO2 and breathed with high rates of oxygen through a circuit connected to the rigid bronchoscope. Total intravenous anesthesia (TIVA) was used for the induction and maintenance of anesthesia in all patients, associated with topical airway anesthesia with lidocaine 2%. All patients with suspected FB inhalation underwent bronchoscopy. From July 1986 to December 2008, only rigid bronchoscopies under general anesthesia were performed. From January 2009 to December 2010, in doubtful cases a flexible bronchoscopy under total intravenous sedation and topical anesthesia was performed to identify the presence of FB and its exact site. During the procedure, the rigid bronchoscopy was anyway ready for use. If negative the endoscopy stopped. If positive, the patient promptly underwent rigid bronchoscopy under general anesthesia to remove the FB. After the removal of the FB, the tracheobronchial tree was investigated for a second time to detect others retained fragments or to look for iatrogenic injury. During the procedure, a dose of intravenous corticosteroids (i.e. betamethasone 0.1 mg/kg die) was always administered. A postoperative aerosol with corticosteroids was done in each patients. If no complications occur, the patients were dismissed the day after the procedure. 3. Results From July 1986 to December 2010, 310 children were admitted to Department of Endoscopic Airways Surgery of Padua Hospital (Italy) from Pediatric Emergency Room for a suspected FB inhalation. One hundred and eighty-four (59.4%) were male and 126 (40.6%) female. The children have an age from 1 month to 14 years (mean age: 2.7 years; median age: 1.6 years). Two hundred and forty-six of the 310 patients (79.4%) were under 3 years of age, while the remaining 64 (20.6%) were older than 3 years. A witnessed inhalation was described in 274 (88.4%) children. All 310 patients were so classified: children with abnormal physical and radiologic findings with symptoms (108 cases), children with abnormal physical findings and normal radiologic findings with symptoms (86 cases), children with normal physical findings and abnormal radiologic findings without symptoms (10 cases), children with normal physical and radiologic findings but with symptoms (74 cases), and children with normal physical and radiologic findings and without symptoms (32 cases).
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Two-hundred and thirty-six (76.2%) patients were referred to our Department within the first 24 h of the event, while 74 (23.8%) patients were admitted and evaluated many hours later. All patients with suspected FB inhalation underwent bronchoscopy. From July 1986 to December 2008, only rigid bronchoscopies under general anesthesia were performed. From January 2009 to December 2010, a flexible bronchoscopy under sedation and topical anesthesia was performed to identify the presence of FB and its exact site. If negative the endoscopy stopped. If positive, the patient underwent rigid bronchoscopy under general anesthesia to remove the FB. So, from January 2009 to December 2010, 30 patients (9.7%) underwent flexible endoscopy to investigate the tracheobronchial tree. Twelve cases of 30 (40%) were negative, stopping the operation and saving the risk of rigid bronchoscopy under general anesthesia. Of 310 evaluations of tracheobronchial tree performed at our department, 104 (33.5%) were negative, while an airway FB were observed and removed in 206 cases (66.5%). Positive cases were male in 123 (59.7%) and female in 83 (40.3%). Most FB were organic in nature in 185 cases (89.8%): 84 (45.4%) peanuts, 23 (12.4%) almonds, 19 (10.3%) walnuts, 10 (5.4%) raw carrots, 6 (3.2%) organic undefined materials, 5 (2.8%) hazelnuts, 5 (2.8%) vegetable fragments, 4 (2.2%) piece of chicken bones, 4 (2.2%) chestnuts, 4 (2.2%) pistachio, 3 (1.6%) food, 2 (1.1%) pieces of apple, 2 (1.1%) maize seeds, 2 (1.1%) sugared almonds, 2 (1.1%) meat fragments, 2 (1.1%) dried fruits, 1 (0.5%) bean seed, 1 (0.5%) piece of fennel, 1 (0.5%) chickpea, 1 (0.5%) lupin, 1 (0.5%) pop corn, 1 (0.5%) seed, 1 (0.5%) pumpkin seed, and 1 (0.5%) orange stem. Inorganic FB were found in 21 patients (10.2%): 8 (38.6%) pieces of plastic, 2 (9.5%) pins, 2 (9.5%) metallic undefined objects, 2 (9.5%) pieces of pen, 1 (4.7%) earring, 1 (4.7%) led, 1 (4.7%) metallic screw, 1 (4.7%) wood fragment, 1 (4.7%) piece of cork, 1 (4.7%) metallic bilia, and 1 (4.7%) rub fragment. In 98 cases of the 206 (47.6%) the FB were located in the right bronchial tree, in 82 (39.8%) in the left bronchial tree, in 13 (6.3%) in trachea, in 5 (2.4%) in larynx (hypoglottic cone), and in 1 case (0.5%) it was wedged in lung. FB of 7 patients (3.4%) was bilateral and was removed from both of the bronchi. In the case of the inhaled FB wedged in lung (it was a pin), rigid bronchoscopy was helpful to localize the FB, but it was impossible to remove the pin with this procedure because it was lodge too peripherally, and the extraction was done by thoracic surgeon with a thoracotomic approach. There were not postoperative major complications. Only reasonable bleeding in 6 patients (2.9%) with sharp or pointed metallic FB lodged or wedged in bronchial mucosa. The bleeding stopped with diluted adrenaline administrated by aerosol. Our complications (such as slight dyspnea or mild laryngeal oedema) were transient and resolved without sequelae with the corticosteroids administered (intravenously and by aerosol).
4. Discussion According to literature, our data showed a prevalence in male [5,9,17,18] younger than 3 years [5,6,12,19], and these may be associated with more activity involved in boys, and the function of protection of epiglottis that is not good/mature in childhood [13]. There are also many others speculations regarding the pathophysiology of FB inhalation: lack of molars necessary for proper grinding of food, tendency of children to explore the environment by placing objects in their oral cavity, inadequate chewing of food, not yet developed neuromuscular mechanisms for swallowing, immaturity of the coordination between swallowing and respiration, and often children play or run or jump or laugh while eating and do not pay attention on chewing and swallowing [12,17].
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According to the literature where the range of finding FB in children with suspected FB aspiration is between 25% and 90% [20], in our study FB were found in 66.5% of the 310 children with a suspected FB inhaled. In addition, according to the literature, most FB inhaled in our data were organic items [9,14,19]. Most frequently, FB were located in the right bronchial tree, probably due to the position of the carina to the left of the midline and its lesser angle of divergence from the tracheal axis [4,17]. A witnessed chocking event is the most important historical information in order to have an early diagnosis of FB inhalation [7]. In literature, it is has been reported to be the most sensitive and specific diagnostic tool and reliable history was noted in 22–86% of patients with suspect of FB aspiration [5]. Paroxysm of coughing and raspy breathing followed by wheezing were the most common presenting symptoms [5]. Other symptoms reported, but uncommon, are tachypnea, nasal flaring, and intercostals and suprasternal retraction [5]. A careful history and physical examination were strong indicators of the diagnosis and raised the index of suspicion of an aspirated FB. Without an adult witness, it can be very difficult to document the acute event, and without confirming history the diagnosis of an FB aspiration may be difficult and may produce any of a variety of symptoms, and the patients may be treated for prolonged periods for asthma, asthmatic bronchitis, bronchiolitis [13], pneumonia, or allergy [12]. Undiagnosed and longstanding retained FB may results in asphyxia, pneumonia, atelectasis, bronchiectasis [9], and lung abscesses [7]. Studies have shown that 50% of patients with an FB inhalation lacked causal history, and 20% of children were misdiagnosed and improperly treated for at last 1 month before the correct diagnosis was made [19]. When FB pass through the trachea in to the bronchi, they may cause partial obstruction of airway and consequent changes in auscultation, including crepitations and wheezes. Unilaterally findings had a higher specificity [16]. Bilaterally findings are less suggestive. Asymmetric decrease in breath sounds and presence of rales were the most frequent findings in patients with FB inhalation, but chest auscultation findings have a poor specificity (26%) [5]. Less common but more specific to FB inhalation is obstructive-induced local hyperinflation or even obstructive emphysema with check-valve mechanism [16]. Symptoms associated to alteration of the vesicular murmur, and the presence of pathological noises upon thoracic auscultation play a fundamental role in planning bronchoscopy [4]. Inhalation of nuts usually determinates more severe signs and symptoms due to local inflammation, oedema, cellular infiltration, ulceration and granular tissue formation that may contribute to airway obstruction [10] and consolidation distal to obstruction. The inflammatory response is much more significant with groundnuts because of their rich in oil [14]. In these cases, bronchoscopic removal is urgent, but it is also difficult identify and remove the organic FB because the airway mucosa becomes more likely to bleed with manipulation [10]. The specificity approached 100% in the presence of witnessed aspiration, chocking, and unilateral decreased breath sounds [14]. Radiography of the airway associated with fluoroscopy can be a useful diagnostic procedure, particularly when it can directly show a FB if is composed of radioopaque material. Moreover sometimes it demonstrate indirect radiological findings of a suspicious FB inhalation such as air trapping, obstructive emphysema, infiltrates and atelectasis, lung hyperinflation, collapse and consolidation, pneumonia, and mediastinal shift [21]. Chest X-ray alone is not sufficient for definitive diagnosis, and radiological evaluation of the airway may not be conclusive [13]. In children with FB in airways, chest radiograph findings are
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frequently normal and can show abnormalities uncharacteristic for FB inhalation [12]. A normal chest radiograph does not exclude a FB and this is seen in nearly two thirds of patients with inhaled FB [11]. In the literature, the most common radiologic finding (60%) is air tripping [5], and normal chest X-ray is present in 18–60% of the patients with FB aspirated. The sensitivity of chest radiograph varied between 60% and 90% in the literature, and had a poor specificity [5]. Although chest X-ray is a quite routine in FB aspiration, it has little value in making the differential diagnosis between FB inhalation and respiratory tract infection [5]. Negative radiography should not preclude bronchoscopy in patients with strongly suggestive history and clinical signs [14]. Since Killian’s first demonstration in 1897 [17], transoral rigid endoscopy has been the gold standard approach to remove airway FB [17]. Many other methods were advocated by some authors, such as balloon-tipped catheters, Foley catheter technique, and flexible fibreoptic endoscopy, but rigid bronchoscopy remains the most widely used technique to remove inhaled FB [12,17]. Flexible bronchoscopy is very helpful in the identification and localization of an airway FB [13]. In clear case of FB inhalation (such as a radioopaque FB, a mediastinal shift, or localized wheezing or decreased lung sounds combined with unilateral atelectasis or hyperinflation [3]) or in case of dyspnea, there is no reason to perform flexible and rigid bronchoscopy, so only the rigid one must be done [20]. Flexible endoscopy is recommended as the appropriate diagnostic tool to eliminate doubt in case of equivocal inhalation (such as doubtful history, with or without doubtful physical examination and negative radiological evaluation) and in case of a first severe asthma attack [22], or acute wheezing [17] or unexplained persistent cough with refractory parenchymal infiltrates, or recurrent pneumonia [20] or other respiratory illness or condition that not respond to appropriate medical management [12]. Only the complete view of tracheobronchial tree can exclude the FB presence. Fibreoptic bronchoscopy showed a diagnostic accuracy rate of 100%, but played a poor therapeutic role [9] and, if positive for FB detection, required a promptly rigid bronchoscopy to remove the tracheobronchial FB. Only in high-qualified centres, as ours (3rd level centre), flexible bronchoscopy with total intravenous sedation and local anesthesia is admitted before the rigid bronchoscopy in order to reduce the risks of a rigid bronchoscopy in those patients with no finding of FB. In our operating room dedicated to endoscopy, the rigid bronchoscopy with a variety of forceps is always present and the surgical team is able to promptly shift from a flexible bronchoscopy into a rigid one in a very short time. A close cooperation between anesthesiologists and otorhinolaryngologists with longstanding experience in pediatric airway emergencies is mandatory to obtain successful results. Furthermore the high experience in airways’ emergencies is essential to not incur possible complications and to reduce the mortality rate of this procedure. Extraction failure and complications are rare [9]. Our complication rate of 2.9% was within the limits stated in literature (2– 22%) [5]. Mani et al. [6] analyzed their 25 years experience and reported that, if child is stable, performing rigid bronchoscopy for suspected FB inhalation during normal working hours preferably on an elective list, under optimal conditions, is safe, does not increase morbidity or mortality and allows optimal conditions for performing the procedure, even if this incurs a delay until the following day. Only if patients are clinically unstable with signs of severe respiratory distress, they go to operative room as an out-ofhours emergency. Prevention is the most critical element in reducing mortality and morbidity [9]. Prevention of aspiration of FB is better than the cure [9]! Public awareness through the mass media should stress
the attention and help prevent FB aspiration [23]. Educational campaigns as a public health measure in some counties have brought down the incidence of FB inhalation and the associated mortality [24,25]. Keeping small objects out of the reach of children and education of older children appears to be the most important way to prevent FB inhalation [26]. Small spherically shaped crunchy food items (such as peanuts, nuts and seeds) are those most likely to cause tracheal obstruction and asphyxia. So, all these foods should be forbidden until the child is able to chew them adequately while sitting. Generally, chewing and swallowing become coordinated around the age of 5 years [9].
5. Conclusions FB aspiration is an uncommon life-threatening event in pediatric patients that can manifest with various symptoms. The patient’s history, symptomatology, and objective chest evaluation are very important for planning bronchoscope. Radiological studies may also add useful information, although cannot exclude FB presence in the airway. A close cooperation between anesthesiologists and otorhinolaryngologists with longstanding experience in pediatric airway emergencies is mandatory to obtain successful results. Rigid bronchoscopy under general anesthesia is an extremely accurate surgical technique to remove FB. In our experience, flexible bronchoscopy under sedation and topical anesthesia is the gold standard to absolutely exclude the presence of FB in tracheobronchial tree in doubtful cases and to correctly identify and localize an airway FB. We agree that prevention must remain the main goal in treating FB inhalation in children. References [1] A. Singh, D. Ghosh, C. Samuel, W. Bhatti, Pediatric foreign body aspiration: how much does our community know? J. Indian Assoc. Pediatr. Surg. 15 (October (4)) (2010) 129–132. [2] B.D. Lifschultz, E.R. Donoghue, Deaths due to foreign body aspiration in children: the continuing hazard of toy balloons, J. Forensic Sci. 41 (2) (1996) 247–251. [3] S. Cohen, A. Avital, S. Godfrey, M. Gross, E. Kerem, C. Springer, Suspected foreign body inhalation in children: what are the indications for bronchoscopy? J. Pediatr. 155 (August (2)) (2009) 276–280. [4] F. Pinzoni, C. Boniotti, S.M. Molinaro, A. Baraldi, M. Berlucchi, Inhaled foreign bodies in pediatric patients: review of personal experience, Int. J. Pediatr. Otorhinolaryngol. 71 (December (12)) (2007) 1897–1903. [5] A.O. Ciftci, M. Bingo¨l-Kolog˘lu, M.E. Senocak, F.C. Tanyel, N. Bu¨yu¨kpamukc¸u, Bronchoscopy for evaluation of foreign body aspiration in children, J. Pediatr. Surg. 38 (August (8)) (2003) 1170–1176. [6] N. Mani, M. Soma, S. Massey, D. Albert, C.M. Bailey, Removal of inhaled foreign bodies – middle of the night or the next morning? Int. J. Pediatr. Otorhinolaryngol. 73 (August (8)) (2009) 1085–1089. [7] K. Wang, A. Harnden, A. Thomson, Easily missed? Foreign body inhalation in children, Clin. Otolaryngol. 35 (December (6)) (2010) 494–495. [8] J.S. Reilly, S.P. Cook, D. Stool, et al., Prevention and management of aerodigestive foreign body injuries in childhood, Pediatr. Clin. North Am. 43 (1996) 1403–1411. [9] D. Passa`li, M. Lauriello, L. Bellussi, G.C. Passali, F.M. Passali, D. Gregori, Foreign body inhalation in children: an update, Acta Otorhinolaryngol. Ital. 30 (February (1)) (2010) 27–32 (Review). [10] A. Chinski, F. Foltran, D. Gregori, D. Passali, L. Bellussi, Foreign bodies causing asphyxiation in children: the experience of the Buenos Aires paediatric ORL clinic, J. Int. Med. Res. 38 (March–April (2)) (2010) 655–660. [11] S. Eren, A.E. Balci, B. Dikici, et al., Foreign body aspiration in children: experience of 1160 cases, Ann. Trop. Paediatr. 23 (2003) 31. [12] I.F. Ozguner, B.I. Buyukyavuz, C. Savas, M.S. Yavuz, H. Okutan, Clinical experience of removing aerodigestive tract foreign bodies with rigid endoscopy in children, Pediatr. Emerg. Care 20 (October (10)) (2004) 671–673. [13] F.L. Tang, M.Z. Chen, Z.L. Du, C.C. Zou, Y.Z. Zhao, Fibrobronchoscopic treatment of foreign body aspiration in children: an experience of 5 years in Hangzhou City, China, J. Pediatr. Surg. 41 (1) (2006) e1–e5. [14] F.T. Orji, J.O. Akpeh, Tracheobronchial foreign body aspiration in children: how reliable are clinical and radiological signs in the diagnosis? Clin. Otolaryngol. 35 (December (6)) (2010) 479–485. [15] N. Saki, S. Nikakhlagh, F. Rahim, H. Abshirini, Foreign body aspirations in infancy: a 20-year experience, Int. J. Med. Sci. 6 (October (6)) (2009) 322–328. [16] G. Kadmon, Y. Stern, E. Bron-Harlev, E. Nahum, E. Battat, T. Schonfeld, Computerized scoring system for the diagnosis of foreign body aspiration in children, Ann. Otol. Rhinol. Laryngol. 117 (November (11)) (2008) 839–843.
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