(Chest. 2005;128:2504-2510.)
© 2005
American College of Chest Physicians
The Role of Timely Intervention in Middle Lobe Syndrome in Children*
Kostas N. Priftis, MD, PhD;
Despina Mermiri, MD;
Athina Papadopoulou, MD, PhD;
Michael B. Anthracopoulos, MD, PhD;
George Vaos, MD, PhD and
Polyxeni Nicolaidou, MD, PhD
* From the Departments of Allergology-Pulmonology (Drs. Priftis, and Mermiri, and Papadopoulou) and Paediatric Surgery (Dr. Vaos), Penteli Children’s Hospital, P. Penteli, Greece; Respiratory Unit (Dr. Anthracopoulos), Department of Paediatrics, University of Patras, Patras, Greece; and the Third Department of Paediatrics (Dr. Nicolaidou), Attikon Hospital, University of Athens School of Medicine, Athens, Greece.
Correspondence to: Kostas N. Priftis, Allergology-Pulmonology Department, Penteli Children’s Hospital, 152 36 P. Penteli, Greece; e-mail: kpriftis{at}otenet.gr
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Abstract
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Study objectives: Middle lobe syndrome (MLS) in children is characterized by a spectrum of clinical and radiographic presentations, from persistent or recurrent atelectasis to pneumonitis and bronchiectasis of the right middle lobe (RML) and/or lingula. This study was undertaken to evaluate the effect of early intervention, including fiberoptic bronchoscopy (FOB), in the development of bronchiectasis in MLS.
Design: Children with atelectasis of the RML and/or lingula persisting for > 1 month or recurring two or more times despite conventional treatment underwent high-resolution CT (HRCT) scanning and FOB. Appropriate treatment and follow-up were provided, and the effect of the duration of symptoms on clinical outcome and the development of bronchiectasis was investigated. The patient cohort was retrospectively reviewed.
Patients: We evaluated 55 children with MLS. The median age at diagnosis, duration of symptoms, and duration of clinical deterioration before diagnosis were 5.5 years (range, 3 months to 12 years), 14.5 months (range, 3 to 48 months), and 8 months (range, 3 to 36 months), respectively.
Measurements and results: FOB revealed marked obstruction in two children (ie, a foreign body and an endobronchial tumor) and positive findings for a culture of BAL fluid in 49.1% of patients. The remaining 53 patients were followed up for a median duration of 24 months (range, 5 to 96 months). The clinical outcome was "cure" in 60.4% of patients, "improvement" in 32.1% of patients, and "no change" in the remaining patients. Bronchiectasis was documented prior to FOB by HRCT scan in 15 patients (27.3%). The duration of the deterioration of symptoms prior to presentation positively correlated with the development of bronchiectasis (p = 0.03) and an unfavorable clinical outcome (ie, improvement or no change) [p = 0.02]; a positive correlation was also found between the duration of symptoms and the development of bronchiectasis (p = 0.04).
Conclusions: Timely medical intervention in patients with MLS that includes FOB with BAL prevents bronchiectasis that may be responsible for an ultimately unfavorable outcome.
Key Words: BAL, bronchiectasis • fiberoptic bronchoscopy • middle lobe syndrome • outcome
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Introduction
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Middle lobe syndrome (MLS) in children is a distinct clinical and radiographic entity that has been well-described in the pediatric literature1234567; however, issues regarding its etiology, clinical presentation, and management continue to puzzle the clinical practitioner. MLS may present as symptomatic or asymptomatic, as persistent or recurrent atelectasis on chest radiographs, or as pneumonitis or bronchiectasis of the right middle lobe (RML) and/or lingula.
Most cases of MLS are considered to be due to asthma, and patients may recover spontaneously.2 However, the recovery from acute symptomatology after an asthma attack may not be accompanied by a concomitant reexpansion of the atelectatic lung parenchyma. Therefore, atelectasis of the RML may persist unnoticed for a prolonged period of time, and repeated episodes of infection/inflammation and obstruction often institute a vicious cycle that may eventually lead to bronchiectasis and on occasion to the need for surgical resection.58910 Consequently, early detection and timely aggressive management of MLS could potentially halt the above-mentioned vicious cycle and result in the reexpansion of the atelectatic region. The appropriate diagnostic evaluation and the correct timing for the initiation of such an endeavor are not clear from the MLS literature at this time. High-resolution CT (HRCT) scanning constitutes to date the state-of-the-art method for diagnosing bronchiectasis,11 and fiberoptic bronchoscopy (FOB) has been recognized as a useful and safe tool in the investigation of infants and children with airway diseases, including persistent atelectasis.12 The objective of the present study was to evaluate the effect of early intervention, including HRCT scanning and FOB, on clinical and radiographic outcomes as well as on the development of bronchiectasis in a cohort of children with persistent or recurrent MLS.
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Materials and Methods
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A retrospective uncontrolled cohort study of children who consecutively presented with MLS and were managed in the Department of Allergology-Pulmonology at Penteli Children’s Hospital between May 1996 and April 2004 was undertaken. MLS was defined as radiographically proven persistent atelectasis (of > 1-month duration) and/or recurrent (ie, two or more episodes) consolidation of the RML and/or lingula; or as the combination of the aforementioned characteristics with atelectasis of other lobes on a plain chest radiograph. Cases of cystic fibrosis (CF), primary ciliary dyskinesia, immunodeficiency, and myoskeletal abnormalities were excluded. Patients with a history consistent with and being evaluated for foreign body aspiration were also excluded. All patients with MLS, as defined above, were placed on an "aggressive" management protocol. They were treated with antibiotics, inhaled bronchodilators, inhaled corticosteroids, and physiotherapy for at least 1 month (range, 4 to 6 weeks); if at that time MLS was not resolved on repeat plain chest radiograph (or recurred, as documented by a third chest radiograph after temporary resolution), patients were evaluated with a detailed history, clinical investigation, and HRCT scan followed by FOB and BAL.
Therapy with antibiotics was discontinued for a minimum of 5 days prior to undergoing FOB. Elective FOB was performed when the child was clinically stable via the nasal route using a 3.6-mm fiberoptic bronchoscope (model BF3C4; Olympus; Tokyo, Japan) under deep sedation with video imaging of the procedure. The bronchoscope was wedged for BAL in a segmental bronchus of the RML or the lingula according to radiographic pathology. BAL was performed with a warmed normal saline solution, and the volume used was adjusted according to body weight using 3 mL/kg divided into three equal aliquots for children weighing < 20 kg, and three 20-mL aliquots for children weighing > 20 kg.13 In all children with bronchiectasis seen on the initial HRCT scan and in selected other patients as per the endoscopist’s judgment, after the initial standardized BAL, repeated "therapeutic" small-volume BAL procedures (3 to 10 mL per aliquot) were performed in the atelectatic bronchi, until clear fluid return was obtained or the lumen was entirely patent in an attempt to reinflate the collapsed lobe.
The cellular component profile of the BAL fluid was evaluated according to the current literature.1314 Values higher than the upper limits of the ranges quoted by Midulla et al14 were considered to be increased. Quantitative cultures for common aerobic and anaerobic bacteria, fungi, and mycobacteria were performed. Samples were considered to be positive for a particular bacterial species if they rendered growth of 
105 cfu/mL or growth of 104 cfu/mL if only one pathogen was isolated that was also associated with the presence of 25% neutrophils. According to the BAL results, in addition to antiasthma treatment and chest physiotherapy, a course of antibiotics for 2 to 4 weeks was prescribed. A new chest radiograph was obtained 4 to 6 weeks after the patient underwent the FOB, and a follow-up HRCT scan was performed 2 to 3 months later to document the persistence or resolution of bronchiectasis. A consultant radiologist reviewed all chest radiographs and HRCT scans.
The definition of MLS and the management protocol described have been agreed on and implemented in our department since 1996. Patients with MLS who had completed the management protocol were enrolled in the study. The follow-up and review of patients for study purposes were performed between February and September 2004, and included a detailed medical history, physical examination, and chest radiograph as needed.
During their course from the time of diagnosis, MLS patients were encouraged to keep simple diaries of their symptoms and to inform the clinic physician of any deterioration in their condition (ie, a new occurrence or an increase in intensity and/or frequency of the symptoms listed in Table 1
); regular monthly telephone contact was maintained. Response to treatment was defined in clinical terms, not roentgenologic terms, as a "cure" if they had experienced three or fewer episodes of cough or wheezing lasting 
7 days each during the 12 months preceding the follow-up and review visit, and as "improvement" if they had experienced fewer episodes per year than during the period before undergoing FOB and the duration of symptoms was 8 to 15 days per episode. The conditions of all of the other patients were considered to be "unchanged." Any outcome other than cure was defined as an "unfavorable clinical outcome." Similarly, an "unfavorable radiographic outcome" was defined as the persistence or incomplete resolution of lesions on repeat HRCT scan. The parents of all study patients and all children 12 years of age gave written informed consent for the FOB. Additional informed consent was obtained for the use of the patients’ records for study purposes. The study protocol was approved by the ethics committee of the hospital.
A statistical software program (SPSS; SPSS Inc; Chicago, IL) was used to analyze clinical, bronchoscopic, and radiographic associations. General descriptive statistics and the significance of differences in clinical and biological features between groups (ie, presence of or no presence of bronchiectasis on HRCT scan and response to the management protocol) were determined using Mann-Whitney U test and/or the 
2 test with Yates correction. Correlation was done with the Spearman test. A two-tailed p value of < 0.05 was considered significant.
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Results
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Fifty-five children (29 male) of 9,524 patients examined in the outpatient clinic of our department during the period of the study fulfilled the inclusion criteria for MLS, and their conditions were managed with HRCT scans and FOB/BAL. All patients were enrolled in the study. The median age at diagnosis was 5.5 years (range, 3 months to 12 years), and the median age at FOB was 5.7 years (range, 4 months to 12.5 years). The median durations of respiratory symptoms and of the deterioration of symptoms before initial presentation to our clinic and the application of our management protocol were 14.5 months (range, 3 to 48 months) and 8 months (range, 3 to 36 months), respectively. Patients were followed up for a median period of 24 months (range, 5 to 96 months) after undergoing FOB. During the same period, 335 children underwent FOB with BAL in our department.
In thirty-two children (58.2%), the chest radiograph that first revealed RML collapse, thus initiating our management protocol, was performed in our department and constituted the first-ever chest imaging investigation of the patient. Table 1 shows the symptoms and the radiographic characteristics of MLS patients. Bronchiectasis was documented at presentation (prior to FOB) by HRCT scan in 15 patients (27.3%).
Bronchoscopic findings, cytology (including differential counts), and quantitative bacterial, mycobacterial, and fungal culture results are presented in Table 2
. A positive culture was found in 49.1% of the 55 individuals enrolled in the study. In 17 samples, only one bacterial pathogen was isolated. Seven samples revealed mixed growth with two bacterial pathogens, and one sample revealed three. One patient had a mixed bacterial-fungal growth, and one patient had a mixed mycobacterial-bacterial growth. None of the 55 study patients had concomitant laryngeal or central airway pathology, such as subglottic stenosis or laryngotracheomalacia. Gastroesophageal reflux was ruled out by esophageal pH study in all seven patients with lipid-laden macrophages in their BAL fluid.
The radiographic and clinical outcomes of patients are presented in Table 3
. Children’s ages and durations of follow-up after FOB were evenly distributed between groups with and without bronchiectasis. The threshold of "early" intervention was set post hoc at 7 months after the deterioration of symptoms; this was the maximum time frame within which the difference between cure and an unfavorable clinical outcome (p = 0.003) and/or radiographic outcome (p = 0.03) of patients treated with our management protocol reached statistical significance. No such threshold could be set for the duration of symptoms. There were no clinical deteriorations during the follow-up period. There was a positive correlation between the duration of symptoms on presentation and bronchiectasis seen on the initial HRCT scan (p = 0.04). There were also positive correlations between the duration of the worsening of symptoms and bronchiectasis on the initial HRCT scan (p = 0.03) and an unfavorable clinical outcome (p = 0.02), and between purulent bronchial discharge (p = 0.03) and positive results of BAL cultures (p = 0.02). Bronchiectasis seen on the initial HRCT scan also correlated with purulent sputum (p = 0.003), purulent bronchial discharge (p = 0.001), lipid-laden macrophages in the BAL fluid (p = 0.001), as well as an unfavorable clinical outcome (p = 0.002) and radiographic outcome (p = 0.001). Other parenchymal involvement, concurrent with MLS, positively correlated with purulent sputum (p = 0.003), purulent bronchial discharge (p = 0.002), and an unfavorable clinical outcome (p = 0.003). No other significant clinical, radiographic, or bronchoscopic/BAL associations were observed. Five of the 21 patients who had an unfavorable response to the management protocol had an increased number of eosinophils; four of these patients had bronchiectasis seen on the initial HRCT scan, none of whom showed a complete radiographic response. All patients with an unfavorable response and increased percentages of eosinophils were treated with at least one burst of oral corticosteroids (1 mg/kg/d prednisolone or its equivalent to a maximum of 40 mg/d) for 5 to 10 days and continued to receive the maximal dose of inhaled corticosteroids throughout the follow-up period.
Figure 1
shows the outcomes of children with and without bronchiectasis at presentation after undergoing FOB and BAL. More patients with a cure outcome belonged to the group without bronchiectasis than to the group with bronchiectasis (p = 0.002). Figure 2
shows pre-FOB and post-FOB plain chest radiographs of a patient with complete resolution of MLS, and Figure 3
shows an example of a patient with MLS who had a complete clinical response, but only partial RML expansion, seen on an HRCT scan after implementation of our management protocol. The only patient who underwent surgical resection (lobectomy) was a 9-year-old girl with seven episodes of "pneumonia" of the lingula within the 2 years prior to our evaluation. A granular cell tumor, causing endobronchial obstruction, was diagnosed. A foreign body detected by FOB in an 11-year-old boy was removed by rigid bronchoscopy under general anesthesia.
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Figure 2.. Left, A: pre-FOB chest radiograph of a 7-year-old boy with a 2-year history of recurrent asthmatic symptoms and a 3-month history of clinical deterioration. Right, B: post-FOB and BAL chest radiograph showing total reexpansion of the RML. The HRCT scan did not reveal bronchiectasis (not shown).
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Figure 3.. RML collapse on pre-FOB chest radiograph (top left, A) and HRCT scan (bottom, B) of a 2.8-year-old girl with a 2-year history of asthmatic symptoms and a 6-month history of clinical deterioration. Top right, C: the chest radiograph obtained after FOB and BAL shows the partial reexpansion of the RML.
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Discussion
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The present study evaluated retrospectively children in whom MLS was diagnosed on chest radiographs whose conditions were managed with a standardized invasive diagnostic and therapeutic protocol. The main finding of the study was the association between the duration of symptoms as well as the duration of the deterioration of symptoms before our intervention, which included intensive conventional management (ie, HRCT scan and FOB with BAL) and an unfavorable clinical and radiographic outcome.
These findings imply a beneficial role of FOB with BAL in the management of patients with MLS. Such a benefit may be the result of the more aggressive and timely conventional management (ie, therapy with antibiotics and antiasthma medication, and physiotherapy) provided by our diagnostic/therapeutic protocol, of the performance of FOB with BAL, which restores the patency of the atelectatic segment per se, or of a combination of these interventions. The proper timing for such aggressive intervention is not known at this time. In our cohort, the aggressive management protocol benefited our patients if it had been instituted within 3 to 7 months from the beginning of the deterioration of symptoms; indeed, the occurrence of deteriorating symptoms for more than 7 months before instituting our "timely, aggressive" intervention was clearly associated with a poorer clinical and radiographic outcome for patients.
The clinical presentation of MLS has not been linked to specific respiratory symptoms but rather to common ones.248 Thus, it is not surprising that such nonspecific symptomatology may result in the underestimation of latently developed atelectasis in anatomically predisposed pulmonary segments. In more than half of our study population, MLS went unnoticed by physicians for an unknown period of time, although symptoms, albeit nonspecific, persisted for many months. A similar diagnostic delay in non-CF bronchiectasis has recently been reported by Eastham et al.11 Therefore, any postponement in obtaining a plain chest radiograph in patients with nonspecific, often mild, persistent respiratory symptoms may result in a failure to diagnose longstanding MLS.141516
Anatomic characteristics, such as the narrow diameter of the lobar bronchus and an acute takeoff angle, make the RML susceptible to transient, usually partial, obstruction. Such obstruction is considered to be the result of the poor drainage of secretions due to inflammation and/or edema of the RML bronchus. In addition, the relative anatomic isolation of the middle lobe and the poor collateral ventilation decrease the chance of reinflation once atelectasis has been established. These mechanisms help to explain the vicious cycle of recurrent inflammation and obstruction that develops after repeated episodes of infection or asthma exacerbations.2489 In our series, complete obstruction of the RML bronchus was found in only three cases (ie, cases of a tumor, a foreign body, and external compression due to enlarged lymph nodes). In the remaining 52 patients, FOB revealed secondary disorders, such as bronchial mucosal edema, scaring, secretions, or, on occasion, mucous plugging; the segmental orifices appeared normal in four patients. Consequently, according to our findings, MLS in children is primarily the result of a nonobstructive process. Similar endoscopic findings have been reported by Livingston et al8; most of the other relevant studies2457 have reported on surgical cases of MLS.
Over half of the children in our study with collapsed middle lobes had an underlying bacterial infection, although none had clinically diagnosed pneumonia. The incidence of infection may have been underestimated due to the use of antibiotics until a few days to a few weeks prior to undergoing the procedure or due to the lack of inclusion of samples with a lighter bacterial growth. The possibility of contamination of BAL fluid samples by oropharyngeal flora cannot be excluded; however, the association of positive culture results with increased neutrophil number and the high number of bacterial colonies set for culture positivity in our samples makes us reasonably confident of the middle lobe origin of the cultured bacteria. The microorganisms detected are those usually isolated in children, most frequently Haemophilus influenzae, followed by Streptococcus pneumoniae and Staphylococcus aureus. H influenzae and S pneumoniae were isolated in frequencies that were similar to those of other studies, while S aureus was more prevalent.911 The association of culture positivity to the duration of worsening of symptoms suggests that infection may hold a pathogenic role in the perpetuation of atelectasis.
The cytologic profile of BAL fluid showed an increased number of eosinophils in 58.2% of the patients, thus strengthening the hypothesis that most of the cases of clinically detected MLS are associated with asthma. In addition, in more than half of the children in the present study an increased number of neutrophils was also detected, which supports the hypothesis of chronic inflammation of the atelectatic lung.23171819 The fact that we were not able to ascribe any cytologic profile to the type of symptoms, to specific endoscopic findings, or to the clinical or radiologic outcome is most likely the result of a number of factors, such as the poor specificity of MLS symptomatology, the administration of antibiotics prior to cultures of BAL fluid, and the coexistence of infection along with the primary cause of the syndrome. The detection of lipid-laden macrophages in seven cases, which was strongly associated with the development of bronchiectasis, is most likely the result of infection rather than aspiration. All patients had normal pH studies, and in six of the seven cases only the RML was affected; however, the possibility of aspiration during swallowing and/or gastric content aspiration despite minimal reflux cannot be dismissed.2021
In their study of the outcome of MLS, De Boeck et al6 did not find any differences in prior conventional management (not including FOB) between symptomatic and asymptomatic patients at the time of follow-up. Our results show that the earlier our management protocol, which included FOB and BAL, was implemented, the lower was the risk of bronchiectatic lesions seen on HRCT scan. On the other hand, we observed that after bronchiectasis has been established, the clinical and radiographic outcomes become less favorable. Bronchiectasis in other lobes of non-CF lung parenchyma has been reported1122 to be of different etiology but due to similar pathogenic mechanisms. The ultimate prognosis probably depends on both etiology and the timing of the therapeutic intervention.1123
In conclusion, the findings of this "pragmatic" study indicate that the nonspecific clinical presentation of MLS in pediatric practice leads to its delayed diagnosis. A lower threshold of performing a plain chest radiograph is warranted in children with persistent or recurrent nonspecific respiratory symptoms, particularly if there is clinical deterioration, in order to detect MLS and to initiate a further diagnostic and therapeutic workup. Medical intervention should focus on the prevention of bronchiectasis, which is associated with ultimately unfavorable clinical and radiographic outcomes. FOB in combination with BAL may be important in achieving a timely diagnosis and may constitute a therapeutic procedure. Our data suggest that FOB and therapeutic BAL should be instituted as soon as possible but definitely should not be delayed > 3 to 7 months from the time that symptom deterioration begins. Prospective studies that address this question are probably worth the effort.
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Footnotes
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Abbreviations: CF = cystic fibrosis; FOB = fiberoptic bronchoscopy; HRCT = high-resolution CT; MLS = middle lobe syndrome; RML = right middle lobe
Received for publication January 5, 2005.
Accepted for publication March 17, 2005.
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References
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Abstract
Introduction
