Abstract
Objectives
Thoracic outlet syndrome, a condition commonly reported in adults, occurs infrequently in the pediatric population. The objective of this study was to assess the outcome of surgical interventions of thoracic outlet syndrome in pediatric patients.
Methods
Clinical records of all pediatric patients with thoracic outlet syndrome who underwent operative repair from 2002 to 2015 in a tertiary pediatric hospital were reviewed. Pertinent clinical variables and treatment outcomes were analyzed.
Results
Sixty-eight patients underwent a total of 72 thoracic outlet syndrome operations (mean age 15.7 years). Venous, neurogenic, and arterial thoracic outlet syndromes occurred in 39 (57%), 21 (31%), and 8 (12%) patients, respectively. Common risk factors for children with venous thoracic outlet syndrome included sports-related injuries (40%) and hypercoagulable disorders (33%). Thirty-five patients (90%) with venous thoracic outlet syndrome underwent catheter-based interventions followed by surgical decompression. All patients underwent first rib resection with scalenectomy via either a supraclavicular approach (n = 60, 88%) or combined supraclavicular and infraclavicular incisions (n = 8, 12%). Concomitant temporary arteriovenous fistula creation was performed in 14 patients (36%). Three patients with arterial thoracic outlet syndrome underwent first rib resection with concomitant subclavian artery aneurysm repair. The mean follow-up duration was 38.4 ± 11.6 months. Long-term symptomatic relief was achieved in 94% of patients.
Conclusions
Venous thoracic outlet syndrome is the most common form of thoracic outlet syndrome in children, followed by neurogenic and arterial thoracic outlet syndromes. Competitive sports-related injuries remain the most common risk factor for venous and neurogenic thoracic outlet syndromes. Temporary arteriovenous fistula creation was useful in venous thoracic outlet syndrome patients in selective children. Surgical decompression provides durable treatment success in children with all subtypes of thoracic outlet syndrome.
Keywords
Introduction
Thoracic outlet syndrome (TOS), a neurovascular bundle compressive disorder affecting the shoulder and neck region, can result in a myriad of upper extremity symptoms including pain, fatigue, paresthesia, pallor, cyanosis, weakness, numbness, limb coldness, heaviness, muscle weakness, and motor deficits. 1 Generally, this condition occurs in adult patients between the age of 25 and 50 years, with a female to male ratio of 3:1. TOS can be categorized into three subtypes, with neurogenic TOS accounting for 95% of cases in adults while venous and arterial TOS make up the remaining 5% of cases.1,2
Our current understanding regarding the clinical condition of TOS is largely derived from the adult literature. In contrast, there is a paucity of clinical experience regarding TOS among pediatric or adolescent patients. The typical neurovascular compressive symptoms of numbness or paresthesia with upper extremity elevation may not be present in these younger patients who may simply describe symptoms of heaviness or dull sensation in the arm or shoulder region. Additionally, pediatric patients may not endure job-related upper extremity repetitive motions which adult patients commonly endure in their employment. Lastly, many children may develop neurovascular compressive symptoms due to a cervical rib or fibrous band, which may be associated with rapid growth spurt.3,4 The infrequent incidence of this condition in younger populations as well as lack of awareness by pediatric healthcare providers often lead to misdiagnosis and delay in treatment. In this report, we examine our clinical experience of TOS in the pediatric population. Surgical treatment and clinical outcomes of these young patients were also analyzed.
Patients and methods
A retrospective review using a prospectively maintained database was performed in all pediatric patients under 18 years of age who underwent surgical treatment for TOS from January 2002 to June 2015. Clinical data were derived from both hospital and clinical records. All surgical procedures were performed by vascular surgical faculty physicians at a large tertiary pediatric hospital. A multidisciplinary group of physicians comprising pediatric hematologist, pediatrician, vascular surgeon, and interventional radiologist were routinely involved in the care of these patients. Appropriate institutional review board approvals were obtained to analyze clinical records and treatment outcomes. Clinical data were gathered which included patient demographics, presenting symptoms, thrombotic risk factors, diagnostic imaging reports, interventional and operative details, anticoagulation therapy, and follow-up notes. Regarding thrombotic risk factors, pertinent data included history of upper extremity activity, prior athletic events, cervical rib, trauma, prolonged abduction, hypercoagulability, illicit drug usage, smoking, or oral contraceptive use. Diagnostic evaluations for these patients varied based on the TOS subtypes. For patients presenting with arteriogenic TOS, upper extremity arterial duplex ultrasound was performed, which was followed by either computed tomography (CT) angiogram or arteriographic evaluation via transfemoral approach. For patients with venous TOS, upper extremity venous duplex ultrasound was the initial study of choice. If upper extremity venous thrombosis was confirmed, these patients then underwent upper extremity venography with thrombectomy and thrombolysis via basilic vein access. Surgical intervention with first rib resection was then performed following endovascular venous intervention, typically during the same hospital course. For patients with neurogenic TOS, various diagnostic modalities including magnetic resonance imaging (MRI), CT scan, and electromyelography (EMG) were utilized to establish the diagnosis.
Follow-up information was obtained from clinical records as well as direct patient contact with survey questionnaires to evaluate the patient’s treatment outcomes. Particular focus from the survey included patient’s activity level, post-surgical rehabilitations, residual TOS symptoms, post-surgical complications, symptoms resolution, analgesic requirement, and ability to return to normal daily or athletic activities. Continuous values are presented as mean ± standard deviation (SD), and categorical variables are listed as numerical values (percentage of those with data available).
Results
A total of 68 patients underwent a total of 70 TOS operations (mean age 15.7 ± 3.7 years). Venous, neurogenic, and arterial TOS occurred in 39 (57%), 21 (31%), and 8 (12%) patients, respectively. Pertinent clinical factors and demographic information are displayed in Table 1. Cervical rib was present in six patients (9%) who developed arterial TOS. Hypercoagulable disorder was identified in 15 children (22%), and 23 patients (34%) developed TOS secondary to sports-related injuries (n = 16, 25%). Three patients (4%) participated in either school band or competitive musical training with instruments which require repetitive upper extremity motion. Specific results of various TOS subtypes are described below.
Patient demographic and pertinent clinical variables of pediatric patients with TOS.
TOS: Thoracic outlet syndrome.
Venous TOS
A total of 40 venous TOS operative procedures were performed in 39 patients. Among them, there were 24 females (62%). Detailed patients’ characteristics and treatment strategies are summarized in Table 2. The most common presenting symptoms were upper extremity swelling (n = 32, 82%), discoloration (n = 27, 69%), and tenderness with pain (n = 15, 38%). At the time of diagnosis, 11 patients (28%) had concurrent neurologic symptoms with either arm paresthesia (n = 7, 18%), pain with arm elevation (n = 3, 8%), or both (n = 1, 3%). Upper extremity venography with thrombectomy or thrombolytic therapy was performed in 35 patients (90%). Complete subclavian vein occlusion was identified in 16 patients (41%). Among them, successful endovascular interventions with thrombolytic therapy or thrombectomy as well as balloon angioplasty was achieved in six patients, while the remaining patients had either persistent subclavian vein occlusion (n = 6) or high-grade residual luminal stenosis (n = 4). Supraclavicular incision was used as the primary surgical approach for first rib resection, scalenectomy, and brachial plexus neurolysis. A combined supraclavicular and sternal infraclavicular incision was needed in three patients (7%) due to medial subclavian vein compression near the sternal junction. A concomitant arteriovenous fistula (AVF) was performed in 14 patients (36%). Among these patients who underwent concomitant AVF creation, eight patients received brachiocephalic AVF while six patients received brachiobasilic AVF creation. Indications for concomitant AVF creations are listed in Table 2. All patients underwent repeat duplex ultrasound to document the recanalization of the subclavian vein. Spontaneous subclavian vein recanalization occurred in all five patients who had subclavian vein occlusion, at a mean postoperative period of 8.6 ± 4.2 months. All patients who underwent concomitant AVF creation also underwent elective AVF ligation with a mean duration of 11.8 ± 5.3 months following the TOS surgery. Four patients (10%) with chronic subclavian vein thrombosis underwent first rib resection without concomitant AVF creation, and three of these patients developed spontaneous subclavian vein recanalization with a mean duration of 16.3 months following the surgical procedure. One remaining patient remained symptom free following first rib resection despite the chronic subclavian vein occlusion. The mean length of hospital stay for venous TOS patients was 8.3 ± 4.8 days. Postoperative complications occurred in one patient (3%) due to atelectasis associated pneumonia.
Summary of clinical variables and treatment strategies of pediatric venous TOS.
TOS: Thoracic outlet syndrome; AV: arteriovenous fistula.
Neurogenic TOS
A total of 22 neurogenic TOS operative procedures were performed in 21 patients. The mean duration from the onset of neurogenic TOS symptoms to surgical treatment was 27.4 ± 5.4. Detailed patients’ characteristics and treatment strategies are summarized in Table 3. The most common presenting symptoms were upper extremity pain exacerbated with arm elevation (n = 14, 67%) and upper extremity numbness (n = 8, 38%). Conservative treatment including physical therapy for a minimum of six months was initiated in all patients. Surgical treatment was considered when physical therapy failed to provide adequate symptomatic relief or when the patient experienced worsening of symptoms. Supraclavicular incision was the preferred operative approach. Combined first rib resection and pectoralis minor tendon release was performed in two patients (9%), while isolated pectoralis minor tendon release was performed in two patients (9%). The mean length of hospital stay for neurogenic TOS patients was 4.7 ± 3.8 days. Postoperative complications occurred in two patients (9%), which included a wound infection (4.7%) and pneumonia (4.7%).
Summary of clinical variables and treatment strategies of pediatric neurogenic TOS.
TOS: Thoracic outlet syndrome.
Arterial TOS
A total of 10 arterial TOS operative procedures were performed in eight patients, including two patients with bilateral symptomatic cervical ribs (Table 4). The most common symptoms of arterial TOS included upper extremity fatigue (n = 4, 50%), hand or finger coldness (n = 3, 38%), or shoulder pain (n = 3, 38%). All the patients had a positive Adson’s test. One patient (13%) developed finger atheroembolism due to subclavian artery aneurysm. CT angiogram (n = 3, 38%), magnetic resonance angiogram (n = 3, 38%)), or angiogram of the subclavian artery (n = 2, 25%) was performed to confirmed subclavian artery compression caused by either first rib (n = 3, 33%) or cervical rib (n = 6, 75%). Supraclavicular incision was utilized in seven cases (70%) to remove the cervical rib alone (n = 4, 40%), first rib alone (n = 3, 30%), or combined first rib and cervical rib (n = 2, 20%). Concomitant scalenectomy and brachial neurolysis were performed in all cases. In three patients with subclavian artery aneurysm due to arterial TOS, interposition bypass grafting of the subclavian artery aneurysm was performed using reversed saphenous vein graft in two patients (20%) and prosthetic expanded polytetrafluoroethylene grafts in one patient (10%). In these patients, combined supraclavicular and infraclavicular incisions were used for subclavian artery reconstruction. The mean length of hospital stay for arterial TOS patients was 6.3 ± 3.5 days. There was no 30-day postoperative complication in these patients.
Summary of clinical variables and treatment strategies of pediatric arterial TOS.
TOS: Thoracic outlet syndrome.
The mean follow-up duration of all patients was 38.4 ± 11.6 months, and four patients (6%) were lost to follow-up. Among the remaining patients, resolution of symptoms within three months occurred in 100% of arterial TOS patients, 87% of venous TOS patients, and 71% of neurogenic TOS patients. No regrowth of the first rib or cervical rib was encountered in our patients. At six months, resolution of symptoms occurred in 100% of arterial TOS patients, 95% of venous TOS patients, and 90% of neurogenic TOS patients, respectively. At one year, complete resolution of symptom occurred in 94% of patients. One patient (1.4%), with antiphospholipid syndrome, developed recurrent subclavian vein thrombosis at 15 months following first rib resection. Catheter-directed thrombolytic therapy was performed which successfully restored the venous flow in the subclavian vein. All patients who sustained sports- or exercise-related injuries were able to resume competitive sports activity following their TOS surgical procedures. Three of the four patients who developed TOS due to musical instrument-associated repetitive motions were able to resume their musical activity.
Discussion
Since TOS was first described by Rob et al. in 1958, 5 this condition has been widely reported in the literature as a potentially debilitating condition primarily affecting the adult population. In contrast, clinical reports of TOS in children are relatively scarce in the literature. Our report is notable as this represents the largest clinical series to date regarding children afflicted with TOS. Additionally, our series showed venous TOS as the most common subtype of TOS rather than the neurogenic condition as seen in adults. This observation has similarly been confirmed by other series.6–8 Lastly, while there is no unified treatment approach in this complex neurovascular compressive disorder, our reports highlight our treatment approach in this pediatric cohort with remarkable treatment outcomes.
Symptoms attributable to vascular TOS account for 69% in our patients. We observe more teenage girls than boys who developed venous TOS. One-fourth of our venous TOS patients experienced sports-related injuries secondary to repetitive overhead strenuous motions involving the affected limb, such as volleyball, softball, and swimming. Additionally, nearly half of our teenage female patients reported concurrent weight lifting exercise as a means to increase their upper extremity strength and muscle growth. These confounding factors, coupled by their rapid body growth in their adolescence, may have contributed to the pathogenesis of venous TOS. The emphasis of athletic sport participation among teenagers, particularly girls, has received heightened awareness in our education system in recent decades, as this has correspondingly been linked to increased incidence of sports-related musculoskeletal injuries.9–11 Similarly, three patients (4%) in our series either participated in the school band or played musical instruments which require repetitive and strenuous upper extremity motion. We recently reported an association of TOS in professional musicians who played stringed instruments such as violin or cello. 12 We postulate these strenuous upper extremity repetitive motions, regardless whether it is sports activity or musical instrument related, can pose undue risk for TOS particularly when these teenagers undergo rapid growth spurts during their adolescent development.
The ideal surgical treatment approach for TOS in adults remains a subject of debate. Understandably, the optimal operative treatment strategy for pediatric TOS remains elusive. Many physicians favor the transaxillary approach because it allows for effective decompression of the vein, permits excellent visualization of the anterior portion of the first rib for resection, and is cosmetically appealing.13–15 In our practice, we prefer a supraclavicular approach for all TOS subtypes for various considerations. First, three patients in our series who had arterial TOS had subclavian artery aneurysm which required first rib resection with concomitant subclavian artery interposition grafting. This procedure required a supraclavicular as well as a lateral infraclavicular incision to gain adequate exposure (Table 4). Transaxillary approach would not provide adequate exposure for subclavian artery reconstruction in terms of proximal and distal vascular control. Second, supraclavicular exposure allows better visualization and enables complete removal of the cervical rib, which was present in six patients (75%) of arterial TOS in our series. Transaxillary approach, in contrast, only provides limited access for cervical rib resection. Third, the neurovascular compression in venous TOS generally occurs at the sternal junction of the clavicle and the first rib secondary to the strenuous hyperabduction of the affected limb. A combined supraclavicular and infraclavicular incisions, or paraclavicular approach, is effective in removing the entire first rib, particularly the medial attachment of the first rib from the sternum. This surgical approach, which was utilized in three patients with venous TOS in our series, has been widely described as the ideal approach to fully alleviate the medial subclavian vein compression with complete detachment of the first rib from the sternal cartilage.16,17 Lastly, transaxillary approach often require either an assistant to elevate and support the upper extremity or customized retractor system for arm elevation during the surgical procedure. These retractor system not only are not available for pediatric patients, but also require intermittent arm lowering to allow periods of increased arterial flow and reduced tension on the stretched nerve. 14 Taken altogether, supraclavicular approach is our preferred incision for TOS patients, particularly in children and adolescent patients.
Our management strategy for venous TOS patients with subclavian vein thrombosis has evolved during the study period. While we routinely performed upper extremity venography and endovascular interventions including thrombectomy or thrombolysis prior to first rib resection, we encountered four patients in our early experience who developed recurrent subclavian vein thrombosis immediately following endovascular intervention. We postulate the small vessel caliber of the affected limb in children may have increased the thrombotic predisposition. The exact timing of first rib resection following angiographic venous intervention is a long debated subject in the literature. Based on their early experience, Machleder et al.18,19 proposed waiting for one to three months before first rib resection to avoid the risk of subclavian vein rethrombosis after surgery with the belief that the venous endothelium will heal and the acute inflammation will resolve. In a subsequent review of their institutional experience, these authors recommended early rib resection following thrombolytic therapy as this would potentially decrease the length of anticoagulation therapy as well as reduce the risk of rethrombosis while awaiting surgical treatment. 20 The benefit of early surgical resection strategy has similarly been confirmed by many clinical reports.13,21–23
Based on these published experiences, we routinely performed early first rib resection, preferably within three days following subclavian venography and intervention. Importantly, we also perform concomitant brachiocephalic AVF creation in the affected limb at the time of first rib resection, particularly in patients with preexisting subclavian thrombosis, to increase the venous flow and promote postoperative subclavian recanalization. These patients would subsequently undergo elective AVF ligation at least three months later or whenever venous duplex ultrasound confirms subclavian vein recanalized patency. In a large series of venous TOS patients who were competitive athletes, Melby et al. 24 reported utilizing this temporary AVF creation strategy in 59% of their patients to increase subclavian venous flow following first rib resection. Five patients (13%) with venous TOS in our series, who had subclavian vein thrombosis, developed spontaneous subclavian vein recanalization with a mean duration of 8.6 months following temporary AVF creation. A potential benefit of the temporary AVF in our pediatric TOS patients is that this may obviate the need for postoperative anticoagulation as many children who could not tolerate subcutaneous lower molecular weight heparin injection since there is no approved pediatric oral anticoagulant medication. We believe the temporary AVF creation is particularly helpful in children whose small vessel diameter may predispose them to postoperative subclavian vein thrombosis. The benefit of temporary AVF creation is also evident in patient with preexisting subclavian vein thrombosis as all of these patients in our series developed recanalized venous patency following first rib decompression.
Similar to adult patients, neurogenic TOS remains a clinical challenge in the pediatric population, due in part to frequent delayed diagnosis and lack of awareness among pediatric healthcare providers. Children or adolescents are less likely to express their symptoms as clearly as adults. Their upper extremity symptoms are also more likely downplayed as being simple muscle strain thereby leading to delay in diagnosis. In our series, the mean duration between the onsets of the neurogenic TOS symptoms to the surgical treatment was 27.4 months, which was in sharp contrast to a mean of 1.8 months in children with venous TOS. Physical examination including provocative maneuvers such as the Adson's test has not proven to be specific for the diagnosis of neurogenic TOS. Other imaging modalities such as MRI, CT, and EMG lack high sensitivity for diagnostic purposes. We routinely pursue conservative treatment including physical therapy as the initial treatment. For those who failed a conservative treatment, surgical decompression with first rib resection with neurolysis is highly effective in children with neurogenic TOS. In our series, resolution of symptoms was usually noted by two months, with more than 90% of patients with neurogenic TOS able to return to exercise or sports activity within one year following surgical treatment.
Undoubtedly, there are several weaknesses in our study. The retrospective design of this analysis incorporated inevitable patient selection and treatment bias. As our series included patients with various subtypes of TOS with each requiring distinctive treatment approach, it is difficult to draw definitive treatment conclusions without randomized treatment strategies. Additionally, the surgical treatment approach was largely based on the treating surgeon’s preference. Consequently, variability in treatment outcomes can exist. Moreover, due to the young age of our patient cohorts, it is difficult to establish a standard treatment protocol for conservative treatment despite the involvement of multidisciplinary pediatric healthcare providers. Lastly, compliance of anticoagulation or exercise regimen for conservative treatment often poses a challenge for children. Notwithstanding these limitations, our treatment resulted in symptomatic relief of nearly all of our TOS pediatric patients.
In conclusion, our series demonstrated that surgical treatment of pediatric TOS can be accomplished with remarkable success in all three subtypes of this condition. When a child or adolescent experiences upper extremity pain, numbness, discomfort, or weakness, healthcare providers should consider the possibility of TOS. Timely diagnosis with appropriate intervention including surgical treatment can lead to successful recovery of both physical and functional capability of the upper extremity. Further study is certainly needed to better delineate the optimal treatment approach in children with TOS.
Footnotes
Acknowledgement
This article was presented at the 35th Annual Meeting of the Southern California Vascular Surgery Society, Rancho Mirage, CA, 5–7 May 2017.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.