- Email: [email protected]
Median arcuate ligament syndrome
Median arcuate ligament syndrome Richard Goodall, BSc, MBChB, FHEA,a,b Benjamin Langridge, MA, MBBS, FHEA,a,b Sarah Onida, BSc, MBBS, MRCS, PhD,a,b Mary Ellis, BSc,a,b Tristan Lane, BSc, MBBS, PhD, FRCS,a,b and Alun Huw Davies, MA, DM, DSc, FRCS, FHEA, FEBVS, FACPh,a,b London, United Kingdom
ABSTRACT Background: Median arcuate ligament syndrome (MALS) describes the clinical presentation associated with direct compression of the celiac artery by the median arcuate ligament. The poorly understood pathophysiologic mechanism, variable symptom severity, and unpredictable response to treatment make MALS a controversial diagnosis. Methods: This review summarizes the literature pertaining to the pathophysiologic mechanism, presentation, diagnosis, and management of MALS. A suggested diagnostic workup and treatment algorithm are presented. Results: Individuals with MALS present with signs and symptoms of foregut ischemia, including exercise-induced or postprandial epigastric pain, nausea, vomiting, and weight loss. Consideration of MALS in patients’ diagnostic workup is typically delayed. Currently, no group consensus agreement as to the diagnostic criteria for MALS exists; duplex ultrasound, angiography, and gastric exercise tonometry are used in different combinations and with varying diagnostic values throughout the literature. Surgical management involves decompression of the median arcuate ligament’s constriction of the celiac artery; robotic, laparoscopic, endoscopic retroperitoneal, and open surgical intervention can provide effective symptom relief, but long-term follow-up data (>5 years) are lacking. Patients treated nonoperatively appear to have worse outcomes. Conclusions: MALS is an important clinical entity with significant impact on affected individuals. Presenting symptoms, patient demographics, and radiologic signs are generally consistent, as is the short-to medium-term (<5 years) response to surgical intervention. Future prospective studies should directly compare long-term symptomatic and quality of life outcomes after nonoperative management with outcomes after open, laparoscopic, endoscopic retroperitoneal, and robotic celiac artery decompression to enable the development of evidence-based guidelines for the management of MALS. (J Vasc Surg 2019;-:1-7.) Keywords: Median arcuate ligament syndrome; Celiac artery compression; Mesenteric ischemia
Median arcuate ligament syndrome (MALS) describes a constellation of clinical signs and symptoms associated with celiac artery compression by the median arcuate ligament (MAL). The true prevalence of MALS is unknown. However, individuals with this phenomenon present with symptoms of foregut ischemia including postprandial or exercise-induced abdominal pain, nausea, and vomiting, with subsequent food aversion and weight loss. In the early 1960s, Harjola1 and Dunbar et al2 demonstrated some relief of symptoms after surgical decompression of the celiac artery in a case report and case series, respectively. However, MALS has since been a topic of contention. Controversy about its existence as a
From the Academic Section of Vascular Surgery, Department of Surgery and Cancer, Imperial College Londona; and the Department of Vascular Surgery, Imperial College Healthcare NHS Trust.b Infrastructure support for this work was supported by the NIHR Imperial Biomedical Research Centre Author conflict of interest: none. Correspondence: Richard Goodall, BSc, MBChB, FHEA, Department of Vascular Surgery, Charing Cross Hospital, 4th Fl, East Wing, Fulham Palace Rd, London W6 8RF, United Kingdom (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2019 by the Society for Vascular Surgery. Published by Elsevier Inc. https://doi.org/10.1016/j.jvs.2019.11.012
syndrome arises from a poorly understood pathophysiologic mechanism, variable presentations (and severity thereof), and unpredictable response to treatment. Accepted universal diagnostic criteria are lacking. Indeed, diagnosis remains one of relative exclusion and is typically the result of extensive (often invasive and radiation-intense) investigations to exclude more common, alternative causes of abdominal pain. Despite this, the European Society for Vascular Surgery (ESVS) clinical practice guidelines for the management of diseases of mesenteric arteries and veins3 recognizes MALS as the most common cause of single-vessel arterial stenosis, with the potential for significant morbidity. This review aimed to outline the anatomy and pathophysiology of MALS. Evidence pertaining to its clinical presentation, diagnosis, and management is reported. A practical algorithm for the management of suspected MALS is presented.
ANATOMY The MAL is a tough fibrous arch connecting the right and left crura of the diaphragm at the level of the aortic hiatus (T12-L1). It traverses anterior to the aorta and is usually cranial to the celiac artery. The position of the MAL and the origin of the celiac artery vary between individuals. A relatively cranial origin of the celiac artery or caudal insertion of the MAL can lead to extrinsic compression of the proximal celiac artery. In 1971, Lindner 1
2
Goodall et al
Journal of Vascular Surgery ---
and Kemprud4 conducted a fresh autopsy study of 75 specimens and noted significant anatomic variability of the MAL. In 33% of patients, the origin of the celiac artery was at or above the level of the MAL. The variation was predominantly due to caudal level and character of the MAL rather than to cranial origin of the celiac artery. This anatomic phenomenon can lead to compression of the celiac artery. The degree of celiac artery compression is subject to respirational variation. In 1973, Reuter and Bernstein5 placed clips on the free edge of the MAL and demonstrated the tendency for ventral movement of the clips and caudal movement of the celiac artery during deep inspiration on lateral aortography, manifested as a tendency to decrease celiac artery compression during deep inspiration and to increase the compression during expiration. Chronic compression by the MAL can lead to hyperplastic intimal changes of the celiac artery. Histologic studies have demonstrated an abundance of smooth muscle proliferation, abnormal elastic fibers, and disorganized medial and adventitial layers that may advance to cause complete arterial occlusion in patients with MALS.6 Downstream of the stenosis, poststenotic dilation and celiac artery aneurysms can complicate MALS further. The visceral artery aneurysm rate in the general population is reported at between 0.1% and 2%; in MALS, it was reported as 48% in a single-center retrospective cohort of 23 patients.7 Of the 11 patients with visceral artery aneurysms, 73% had aneurysmal disease in the pancreaticoduodenal arcade, 27% in the splenic artery, and 18% in the celiac artery. Furthermore, the proximity of the celiac ganglion to the compressed celiac artery and evidence of symptomatic benefit after interventions targeting the celiac ganglion8 have led to postulations that neuropathic pain is a contributory factor in MALS. The mechanism for this is thought to be compression of the celiac ganglion by the MAL and subsequent overstimulation of pain fibers of the sympathetic nervous system.6
PRESENTATION The true prevalence of MALS is unclear, which is partly due to its variable clinical presentation. There is a tendency toward a female phenotype (4:1), and the median age typically lies between 30 and 50 years.9 Cases have also been reported in pediatric populations.10 Frequently reported symptoms include epigastric pain, nausea, vomiting, weight loss, and postprandial or exercise-induced abdominal pain. Clinical signs may include abdominal bruits (amplified with expiration), epigastric tenderness, and marked weight loss. In a case series of 43 individuals treated surgically for MALS11 (defined in the study as the presence of unexplained chronic abdominal symptoms and angiographic evidence of >50% compression of the proximal celiac
2019
artery), the pretreatment clinical features included abdominal pain in 91% of patients (which was postprandial in 62%, postexertional in 32%, and unprovoked in 33%). In addition, 40% of individuals had weight loss, 30% had nausea, and 47% had audible epigastric bruits. In a retrospective cohort12 of 344 asymptomatic individuals undergoing computed tomography angiography (CTA) before live kidney donation, evidence of celiac artery compression of >50% by the MAL was reported in 3.4% of individuals. Furthermore, in a retrospective database analysis13 of 744 patients in whom CTA was performed for various indications, radiologic evidence of celiac artery compression by the MAL was present in 2.8% of cases. Interestingly, only three patients with radiologic evidence of celiac artery compression presented with symptoms of MALS. This retrospective study probably under-reported the true symptom rate, but an additional explanation for the lack of symptoms in patients with radiologic evidence of MALS may be the development of collateral circulation. Heo et al14 demonstrated collateral circulation in 46% of their cohort of 32 asymptomatic patients with radiologic evidence of MALS. Intriguingly, ska et al15 noted a significantly positive correlation Arazin between the degree of celiac artery stenosis and the presence of collateral circulation (Spearman correlation coefficient ¼ 0.339; P < .001) on CTA. An emerging theme in the literature is the presence of psychiatric comorbidities in a significant proportion of patients with MALS. In a prospective observational analysis16 of 51 patients undergoing surgical intervention for MALS (defined as chronic abdominal pain with radiologic evidence of extrinsic celiac artery compression and altered celiac artery hemodynamics), 28% of patients demonstrated preoperative symptoms consistent with a psychiatric disorder according to criteria from the Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition, Text Revision). Anxiety disorders predominated, a theme that appears consistent.16-18 Pediatric patients also appear vulnerable to the coexistence of MALS and psychiatric disorders. Mak et al18 demonstrated similar pediatric psychosocial profiles (notably a high incidence of anxiety and mood disorders) in patients with MALS to patients with other gastrointestinal disorders resulting in chronic abdominal pain, including inflammatory bowel disease. Reilly et al19 concluded from their 1985 case series with a 9-year mean follow-up that improved surgical outcomes correlated with lack of psychiatric history. Similarly, Skelly et al16 concluded that a preoperative psychiatric diagnosis predicted a lower postsurgical overall quality of life. Analysis of the raw data from the prospective observational analysis of Skelly et al, however, suggests alternative conclusions. Patients with a coexistent psychiatric diagnosis had a significantly lower overall quality of life score preoperatively compared with those without psychiatric diagnoses. Intriguingly,
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
3
-
Fig 1. Diagnostic imaging. A, Duplex ultrasound (DUS) image (in expiration) of the abdominal aorta revealing steep angulation of the celiac axis (arrow). Orientation: cranial end to the right of the image. B, Sagittal threedimensional volume-rendered image of the abdominal aorta demonstrating narrowing and angulation of proximal celiac artery (arrow).
the overall difference in quality of life scores actually was reduced postoperatively from 12.9 points (P ¼ .007) to 11.3 points (P ¼ .01), suggesting a relatively greater improvement in overall quality of life in those with a preexistent psychiatric disorder. A large dropout rate of 44 of a total 95 patients operated on for MALS also limits reliable conclusions from this study.
DIAGNOSIS Diagnosis of MALS typically depends on exclusion of alternative causes of abdominal pain. Indeed, before investigation for MALS, a formal gastroenterology review is advisable to rule out more common explanations for the patients’ symptoms; esophagogastroduodenoscopy, colonoscopy, motility studies, and cross-sectional imaging and relevant hematologic studies should be obtained. The ESVS clinical practice guideline on the management of mesenteric disease3 provides recommendations as how best to investigate patients with suspected chronic mesenteric ischemia. The guideline refers to MALS in the chronic mesenteric ischemia section and recognizes MALS as the most common cause of single mesenteric vessel stenosis. However, the document also states that the symptoms observed in MALS may not be caused by chronic mesenteric ischemia; therefore, the ensuing diagnostic and treatment recommendations in the guideline, which are based predominantly on chronic mesenteric ischemia resulting from multivessel stenotic disease of an atherosclerotic pathophysiologic process, have limited applicability to MALS. To the authors’ knowledge, no other group consensus agreement as to the diagnosis of MALS exists. Unremarkable findings on abdominal ultrasound, computed tomography, and upper gastrointestinal endoscopy are common in patients with MALS. When
clinical suspicion of chronic mesenteric ischemia arises, duplex ultrasound (DUS) is the first-line recommended investigation3 (Fig 1). DUS is advantageous as an initial investigation compared with angiography as it is cheaper and noninvasive, and it does not expose patients to high doses of radiation. Gruber et al20 conducted a retrospective cohort study of 364 patients undergoing DUS of the celiac trunk. Of the six patients with a retrospective diagnosis of MALS (based on chronic abdominal symptoms and angiographic evidence of celiac artery stenosis with extrinsic compression), 100% had celiac trunk deflection angles of >50 degrees compared with 40% in the asymptomatic control group (8/20 patients). Their analysis demonstrated significant differences in expiratory peak systolic flow velocities (PSVs) in the patients with MALS (mean PSV, 425 6 130.1 cm/s) compared with asymptomatic controls (mean PSV, 209.9 6 80.1 cm/s; two-tailed Mann-Whitney U, P ¼ .001). They concluded that a combination of a deflection angle >50 degrees and an expiratory PSV of >350 cm/s confers 83% sensitivity, 100% specificity, and 100% positive predictive value for a diagnosis of MALS in their patient group. Data were obtained from a small sample size (n ¼ 14), however, and the possibility of interobserver and intraequipment variability must also be considered. CTA is an additional noninvasive imaging tool to diagnose arterial occlusion. Three-dimensional images of the mesenteric arteries, the position of the MAL, and imaging able to detect differential diagnoses are rapidly acquired. The ESVS guideline3 states that in patients in whom there is a moderate to high suspicion of chronic mesenteric ischemia, CTA is recommended to map occlusive disease and to detect or to exclude other intra-abdominal disease. CTA features in MALS include focal narrowing of the proximal celiac artery with a characteristic hooked appearance.21 This “hooking” helps
4
Journal of Vascular Surgery
Goodall et al
---
differentiate MALS stenosis from atherosclerotic narrowing. CTA also permits better appreciation of poststenotic dilation and visceral artery aneurysms compared with DUS. On the contrary, changes in vessel caliber and flow velocity with respiration are more easily appreciated with DUS. Magnetic resonance angiography and digital subtraction angiography (DSA) can provide similar appreciation of vessel stenosis as CTA. Angiography also permits appreciation of the degree of collateralization accompanying the celiac artery stenosis. This may be of clinical importance with respect to predicting the patient’s response to treatment. van Petersen et al22 performed a retrospective analysis of 129 patients with MALS (diagnosed as chronic unexplained abdominal pain, radiologic evidence of extrinsic celiac artery compression, and objective evidence of gastric ischemia on tonometry) who underwent decompression of the MAL through retroperitoneal open or endoscopic techniques. The authors demonstrated that individuals with extensive collateral mesenteric circulation (classified as at least one collateral clearly visible on nonselective DSA) are less likely to benefit from MAL release compared with individuals with no or less extensive collateralization (ie, no visible collaterals or collaterals visible on selective DSA but not visible on nonselective DSA). Magnetic resonance angiography, DSA, and CTA should be performed in inspiration and expiration to demonstrate the changes in celiac artery compression with the phases of respiration. Interestingly, a convincing correlation between degree of angiographic stenosis and likelihood of being symptomatic from MALS is lacking. Stenosis of >50% of the celiac artery produced symptoms in only 1 of 8 patients in a retrospective observational study of >1000 individuals who underwent CTA.23 Gastric exercise tonometry (GET) is reported to be 76% sensitive and 92% specific for the diagnosis of intestinal ischemia.24,25 A positive GET study results from a rising intraluminal partial pressure of carbon dioxide from anaerobic respiration. In a prospective cohort study, Mensink et al26 demonstrated positive GET results in 29 of 43 patients with abdominal pain and significant celiac artery compression (stenosis of >70% visible on DSA). Patients then underwent MAL release (22 patients underwent MAL release alone and 7 patients received MAL release with celiac artery reconstruction). At a median follow-up of 39 months, those who were symptom free (83%) had normal findings on GET, whereas abnormal GET results persisted in 25% of patients with ongoing symptoms (P < .001). They concluded that this suggested that MALS was an ischemic syndrome and that surgical intervention can effectively treat the ischemic phenomenon, which would in turn be manifested as resolution of symptoms. However, the remaining 13 symptomatic patients with positive DSA and negative GET results did not receive surgical MAL release,
2019
which limits important comparisons. Moreover, despite its apparently high diagnostic accuracy, GET is not ubiquitous and is a complicated and time-intense procedure. The contribution of compression of the celiac plexusdwhich conveys foregut visceral afferent pain sensationdby the MAL has also been suggested by some as a diagnostic target in MALS.27,28 Weber et al27 performed preoperative, temporary percutaneous celiac plexus block using a local anesthetic agent in four patients with radiologic evidence of MALS with atypical symptoms; 100% of these patients described symptom relief after the block, and all reported symptom relief after subsequent laparoscopic decompression. Indeed, a positive response to a diagnostic celiac plexus block may predict good response to surgical decompression and celiac ganglionectomy; however, quality evidence to support this statement is lacking. Moreover, evidence demonstrating the differential benefits of celiac ganglion block in individuals with chronic unexplained abdominal pain and radiologic evidence of MALS, with vs without GET results positive for ischemia, is lacking. An understanding of the differing contribution of the celiac plexus to symptoms across the MALS disease spectrum represents an area for future research to improve targeted therapy.
MANAGEMENT Interventions for MALS aim to address the hypothesized pathophysiologic mechanisms: decompression of the MAL’s constriction of the celiac artery, with or without celiac ganglionectomy to target the neuropathic component to the pain. Fig 2 demonstrates a suggested diagnosis and treatment algorithm for patients with suspected MALS based on review of the currently available literature. Decompression of the celiac artery was traditionally achieved through an open approach, in which a chevron or upper midline laparotomy permits identification of the MAL and celiac artery. The compressive band is then divided, along with division and wide excision of the celiac ganglion (ganglionectomy), and the proximal celiac artery is completely exposed. Celiac ganglionectomy rather than simple neurolysis is recommended as a means of addressing the neuropathic pain associated with MALS. Recent years, however, have seen a trend toward laparoscopic intervention to decompress the celiac artery. Endovascular intervention alone does not address the extrinsic compression of the celiac artery and has subsequently proven ineffective as an isolated treatment of MALS.9 Persistent stenosis of the celiac artery after decompression may be appreciated with intraoperative handheld Doppler assessment, angiography, or DUS. This can be addressed with arterial reconstruction, examples of which include an aortoceliac bypass or a celiac artery patch angioplasty. Conversion from laparoscopic to
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
5
-
Fig 2. Median arcuate ligament syndrome (MALS) diagnosis and management. Flow chart demonstrating suggested diagnostic workup and management for patients with MALS. CTA, Computed tomography angiography; DSA, digital subtraction angiography; MAL, median arcuate ligament; MRA, magnetic resonance angiography.
open surgery is typically required for vascular reconstruction. Percutaneous transluminal angioplasty with or without stenting provides an adjunctive endovascular approach to revascularization of a persistent stenosis after MAL release. Jiminez et al29 performed a review of studies reporting on outcomes of surgical interventions for MALS. Twenty studies reporting data from 400 patients undergoing surgical intervention for MALS were included; 279 underwent open MAL division, and 121 received laparoscopic division. Follow-up duration ranged from 10 to 229 months for the open group and 6 to 44 months for the laparoscopic group. The majority of included studies reported data on fewer than 20 patients, with a followup of <3 years. Overall, 85% of patients reported immediate postoperative symptom relief (open group, 78%; laparoscopic group, 96%). Late recurrence rates were 6.8% for patients treated with open MAL division and
5.7% for patients treated laparoscopically; 9.1% of laparoscopic procedures were converted to open surgery because of bleeding. Quality of life outcomes and comparisons of adverse event data were lacking; however, the study states that no procedure-related or early perioperative deaths were reported. Only one of the studies30 included in the review directly compared open MAL release and ganglionectomy (n ¼ 6) with laparoscopic MAL release and ganglionectomy (n ¼ 8) in a cohort of patients with chronic unexplained abdominal pain and radiologic evidence of extrinsic compression of the MAL. The authors concluded that both procedures can be safely performed with minimal morbidity. They noted significant differences only for the length of hospital stay (laparoscopic group, 2.3 days; open group, 7.0 days; P # .05) and time to feeding (open group, 2.8 days; laparoscopic group, 1.0 days; P # .05), both of which were better in the laparoscopic
6
Journal of Vascular Surgery
Goodall et al
---
group. A small sample size (14 patients) and short median follow-up duration (14.0 months) limit conclusions from this study. Moreover, two of the patients in the laparoscopic group required conversion to open surgery because of intraoperative bleeding. Endoscopic retroperitoneal approaches to MAL release have also been reported. In a case series of 46 individuals with a diagnosis of MALS31 (based on positive symptoms, angiographic evidence of celiac artery compression, and GET results positive for ischemia), 89% of patients reported either symptom resolution or significant improvement at a median follow-up of 20 months. Only one patient required conversion to laparotomy (because of bleeding from the suprarenal artery), and pneumothorax occurred in three individuals. No other complications were reported, and the mean hospital stay was 5.6 days. Ho et al11 compared outcomes of surgical intervention (laparoscopic [n ¼ 38] or open [n ¼ 5] MAL release) with nonoperative management for MALS. A diagnosis of MALS was made on the basis of symptoms of chronic abdominal pain and radiologically confirmed extrinsic compression of the celiac artery (GET was not part of the diagnostic workup). They reported symptom resolution or improvement in 95% of patients in the surgical group (n ¼ 43) compared with 33% in the nonoperative group (n ¼ 24) after a retrospective review. However, group differences limit reliable comparisons. Notable differences included more patients with celiac artery stenosis >70% (surgical group, 62%; nonoperative group, 36%) and fewer patients with unprovoked abdominal pain (surgical group, 33%; nonoperative group, 64%) in the surgical group compared with the nonoperative group. Robot-assisted MAL release and celiac ganglionectomy represents an emerging treatment modality for individuals with MALS. Do et al32 found that laparoscopic MAL release had significantly shorter operative times than robot-assisted laparoscopic release but concluded that both are safe and effective interventions in their retrospective cohort of 16 patients with unexplained chronic abdominal symptoms and celiac artery compression. Direct, randomized comparisons of MAL release with and without arterial revascularization (in the form of celiac artery reconstruction or percutaneous transluminal angioplasty) are lacking. Schweizer et al33 presented a retrospective case series of eight pediatric patients with MALS (diagnosis based on symptoms of chronic abdominal pain and an audible epigastric bruit) who underwent surgical MAL release without any form of arterial revascularization, and all were symptom free at the end of follow-up (follow-up range, 3-18 years). Furthermore, van Petersen et al22 performed MAL release through an endoscopic retroperitoneal approach in 46 patients with symptoms and GET evidence of ischemia. In 36 of these patients, arterial reconstruction or endovascular revascularization was not performed. At a median follow-up of 20 months, 89% of all patients were free of
2019
symptoms or showed significant symptomatic improvement. On the contrary, a retrospective cohort34 of eight adult individuals with MALS treated with open MAL release and celiac ganglionectomy without arterial revascularization had a 100% symptom recurrence rate at the end of follow-up (mean, 19.1 years). Predicting the patients in whom arterial reconstruction would offer benefit represents an ongoing challenge in the management of MALS. Moving forward, the published interventional research suggests that clinical equipoise likely exists to permit direct, prospective, perhaps even randomized comparisons of open, laparoscopic, endoscopic retroperitoneal, and robot-assisted decompression of the celiac artery for treatment of MALS. Given the relative rarity of MALS presentation, a multicenter collaborative trial would likely be appropriate to obtain adequate patient numbers. Prospective studies might consider including targeted psychiatric interventions as an adjunct to surgical management, and the diagnostic value of preoperative percutaneous celiac plexus block represents an additional area for investigation. Emphasis should be placed on better classification of individuals likely to respond to surgical intervention and clarification of the roles of celiac ganglionectomy and arterial revascularization in disease management. Robust comparisons of length of hospital stay, adverse events, reintervention rates, persistence of celiac artery stenosis, and, importantly, long-term symptom relief resulting from each of the surgical approaches should be presented.
CONCLUSIONS The available evidence is highly suggestive that MALS exists. Despite no definitive group consensus agreement as to the diagnostic criteria or management of MALS, patient presentation and radiologic signs appear generally consistent across the literature. Moreover, recent procedural studies agree that surgical intervention can treat this controversial but debilitating condition. Currently, however, inadequate long-term (>5 years) follow-up data limit assumptions as to whether surgery is effective for treatment of MALS. Consensus as to the optimal surgical approach to management is also lacking. Despite this, an increased awareness of MALS would permit earlier consideration and investigation of the syndrome as part of a diagnostic workup for patients with symptoms of abdominal pain and weight loss not attributable to more common conditions.
AUTHOR CONTRIBUTIONS Conception and design: RG, BL, SO, AD Analysis and interpretation: RG, SO, ME, TL, AD Data collection: Not applicable Writing the article: RG, BL, SO Critical revision of the article: RG, BL, SO, ME, TL, AD Final approval of the article: RG, BL, SO, ME, TL, AD
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
7
-
Statistical analysis: Not applicable Obtained funding: Not applicable Overall responsibility: AD
REFERENCES 1. Harjola PT. A rare obstruction of the celiac artery. Ann Chir Gynaecol Fenn 1963;52:547-50. 2. Dunbar JD, Molnar W, Beman FF, Marable SA. Compression of the celiac trunk and abdominal angina. Am J Roentgenol Radium Ther Nucl Med 1965;95:731-44. 3. Bjork M, Koelemay M, Acosta S, Bastos Goncalves F, Kölbel T, Kolkman JJ, et al. Management of the diseases of mesenteric arteries and veins. Eur J Vasc Endovasc Surg 2017;53: 460-510. 4. Lindner HH, Kemprud E. A clinicoanatomical study of the arcuate ligament of the diaphragm. Arch Surg 1971;103: 600-5. 5. Reuter SR, Bernstein EF. The anatomic basis for respiratory variation in median arcuate ligament compression of the celiac artery. Surgery 1973;73:381-5. 6. Bech FR. Celiac artery compression syndromes. Surg Clin North Am 1997;77:409-24. 7. Nasr LA, Faraj WG, Al-Kutoubi A, Hamady M, Khalifeh M, Hallal A, et al. Median arcuate ligament syndrome: a singlecenter experience with 23 patients. Cardiovasc Intervent Radiol 2017;40:664-70. 8. Sultan S, Niamh H. PS160. Management of median arcuate ligament syndrome (MALS) with decompression and coeliac ganglion sympathectomy (CGS) for chronic mesenteric ischaemia (CMI). Procedural, clinical and enduring results with quality-adjusted time spent without symptoms of disease and toxicity of treatment (Q-TWiST). J Vasc Surg 2010;51:62S. 9. Kim EN, Lamb K, Relles D, Moudgill N, DiMuzio PJ, Eisenberg JA. Median arcuate ligament syndromedreview of this rare disease. JAMA Surg 2016;151:471-7. 10. Scholbach T. Celiac artery compression syndrome in children, adolescents, and young adults: clinical and color duplex sonographic features in a series of 59 cases. J Ultrasound Med 2006;25:299-305. 11. Ho KK, Walker P, Smithers BM, Foster W, Nathanson L, O’Rourke N, et al. Outcome predictors in median arcuate ligament syndrome. J Vasc Surg 2017;65:1745-52. 12. Petnys A, Puech-Leão P, Zerati AE, Ritti-Dias RM, Nahas WC, Neto ED, et al. Prevalence of signs of celiac axis compression by the median arcuate ligament on computed tomography angiography in asymptomatic patients. J Vasc Surg 2018;68: 1782-7. 13. Gümüs H, Gümüs M, Tekbas G, Önder H, Ekici F, Cetinçakmak MG, et al. Clinical and multidetector computed tomography findings of patients with median arcuate ligament syndrome. Clin Imaging 2012;36:522-5. 14. Heo S, Kim HJ, Kim B, Lee JH, Kim J, Kim JK. Clinical impact of collateral circulation in patients with median arcuate ligament syndrome. Diagn Interv Radiol 2018;24:181-6. ska A, Polguj M, Wojciechowski A, Trębin ski q, 15. Arazin czyk L. Median arcuate ligament syndrome: predictor Stefan of ischemic complications? Clin Anat 2016;29:1025-30. 16. Skelly C, Stiles-Shields C, Mak GZ, Speaker CR, Lorenz J, Anitescu M, et al. The impact of psychiatric comorbidities on patient-reported surgical outcomes in adults treated for the median arcuate ligament syndrome. J Vasc Surg 2018;68: 1414-21. 17. Columbo J, Trus T, Nolan B, Goodney P, Rzucidlo E, Powell R, et al. Contemporary management of median arcuate
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
ligament syndrome provides early symptom improvement. J Vasc Surg 2015;62:151-6. Mak G, Speaker C, Anderson K, Stiles-Shields C, Lorenz J, Drossos T, et al. Median arcuate ligament syndrome in the pediatric population. J Pediatr Surg 2013;48:2261-70. Reilly LM, Ammar AD, Stoney RJ, Ehrenfeld WK. Late results following operative repair for celiac artery compression syndrome. J Vasc Surg 1985;2:79-91. Gruber H, Loizides A, Peer S, Gruber I. Ultrasound of the median arcuate ligament syndrome: a new approach to diagnosis. Med Ultrason 2012;14:5-9. Horton KM, Talamini MA, Fishman EK. Median arcuate ligament syndrome: evaluation with CT angiography. Radiographics 2005;25:1177-82. van Petersen AS, Kolkman JJ, Gerrits DG, van der Palen J, Zeebregts CJ, Geelgerken RH, et al. Clinical significance of mesenteric arterial collateral circulation in patients with celiac artery compression syndrome. J Vasc Surg 2017;65: 1366-74. Baskan O, Kaya E, Gungoren FZ, Erol C. Compression of the celiac artery by the median arcuate ligament: multidetector computed tomography findings and characteristics. Can Assoc Radiol J 2015;66:272-6. Otte JA, Geelkerken RH, Oostveen E, Mensink PB, Huisman AB, Kolkman JJ. Clinical impact of gastric exercise tonometry on diagnosis and management of chronic gastrointestinal ischemia. Clin Gastroenterol Hepatol 2005;3: 660-6. Sana A, Vergouwe Y, van Noord D, Moons LM, Pattynama PM, Verhagen HJ, et al. Radiological imaging and gastrointestinal tonometry add value in diagnosis of chronic gastrointestinal ischemia. Clin Gastroenterol Hepatol 2011;9:234-41. Mensink PB, van Petersen AS, Kolkman JJ, Otte JA, Huisman AB, Geelkerken RH. Gastric exercise tonometry: the key investigation in patients with suspected celiac artery compression syndrome. J Vasc Surg 2006;44:277-81. Weber JM, Boules M, Fong K, Abraham B, Bena J, El-Hayek K, et al. Median arcuate ligament syndrome is not a vascular disease. Ann Vasc Surg 2016;30:22-7. Gloviczki P, Duncan AA. Treatment of celiac artery compression syndrome: does it really exist? Perspect Vasc Surg Endovasc Ther 2007;19:259-63. Jiminez JC, Harlander-Locke M, Dutson EP. Open and laparoscopic treatment of median arcuate ligament syndrome. J Vasc Surg 2012;56:869-73. Tulloch AW, Jiminez JC, Lawrence PF, Dutson EP, Moore WS, Rigberg DA, et al. Laparoscopic versus open celiac ganglionectomy in patients with median arcuate ligament syndrome. J Vasc Surg 2010;52:1283-9. van Petersen AS, Vriens BH, Huisman AB, Kolkman JJ, Geelkerken RH. Retroperitoneal endoscopic release in the management of celiac artery compression syndrome. J Vasc Surg 2009;50:140-7. Do MV, Smith TA, Bazan HA, Sternbergh WC 3rd, Abbas AE, Richardson WS. Laparoscopic versus robot-assisted surgery for median arcuate ligament syndrome. Surg Endosc 2013;27:4060-6. Schweizer P, Berger S, Schweizer M, Schaefer J, Beck O. Arcuate ligament vascular compression syndrome in infants and children. J Pediatr Surg 2005;40:1616-22. Geelkerken RH, Van Bockel JH, De Roos WK, Hermans J. Br J Surg 1990;77:807-9.
Submitted Jul 29, 2019; accepted Nov 3, 2019.
ABSTRACT Background: Median arcuate ligament syndrome (MALS) describes the clinical presentation associated with direct compression of the celiac artery by the median arcuate ligament. The poorly understood pathophysiologic mechanism, variable symptom severity, and unpredictable response to treatment make MALS a controversial diagnosis. Methods: This review summarizes the literature pertaining to the pathophysiologic mechanism, presentation, diagnosis, and management of MALS. A suggested diagnostic workup and treatment algorithm are presented. Results: Individuals with MALS present with signs and symptoms of foregut ischemia, including exercise-induced or postprandial epigastric pain, nausea, vomiting, and weight loss. Consideration of MALS in patients’ diagnostic workup is typically delayed. Currently, no group consensus agreement as to the diagnostic criteria for MALS exists; duplex ultrasound, angiography, and gastric exercise tonometry are used in different combinations and with varying diagnostic values throughout the literature. Surgical management involves decompression of the median arcuate ligament’s constriction of the celiac artery; robotic, laparoscopic, endoscopic retroperitoneal, and open surgical intervention can provide effective symptom relief, but long-term follow-up data (>5 years) are lacking. Patients treated nonoperatively appear to have worse outcomes. Conclusions: MALS is an important clinical entity with significant impact on affected individuals. Presenting symptoms, patient demographics, and radiologic signs are generally consistent, as is the short-to medium-term (<5 years) response to surgical intervention. Future prospective studies should directly compare long-term symptomatic and quality of life outcomes after nonoperative management with outcomes after open, laparoscopic, endoscopic retroperitoneal, and robotic celiac artery decompression to enable the development of evidence-based guidelines for the management of MALS. (J Vasc Surg 2019;-:1-7.) Keywords: Median arcuate ligament syndrome; Celiac artery compression; Mesenteric ischemia
Median arcuate ligament syndrome (MALS) describes a constellation of clinical signs and symptoms associated with celiac artery compression by the median arcuate ligament (MAL). The true prevalence of MALS is unknown. However, individuals with this phenomenon present with symptoms of foregut ischemia including postprandial or exercise-induced abdominal pain, nausea, and vomiting, with subsequent food aversion and weight loss. In the early 1960s, Harjola1 and Dunbar et al2 demonstrated some relief of symptoms after surgical decompression of the celiac artery in a case report and case series, respectively. However, MALS has since been a topic of contention. Controversy about its existence as a
From the Academic Section of Vascular Surgery, Department of Surgery and Cancer, Imperial College Londona; and the Department of Vascular Surgery, Imperial College Healthcare NHS Trust.b Infrastructure support for this work was supported by the NIHR Imperial Biomedical Research Centre Author conflict of interest: none. Correspondence: Richard Goodall, BSc, MBChB, FHEA, Department of Vascular Surgery, Charing Cross Hospital, 4th Fl, East Wing, Fulham Palace Rd, London W6 8RF, United Kingdom (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 0741-5214 Copyright Ó 2019 by the Society for Vascular Surgery. Published by Elsevier Inc. https://doi.org/10.1016/j.jvs.2019.11.012
syndrome arises from a poorly understood pathophysiologic mechanism, variable presentations (and severity thereof), and unpredictable response to treatment. Accepted universal diagnostic criteria are lacking. Indeed, diagnosis remains one of relative exclusion and is typically the result of extensive (often invasive and radiation-intense) investigations to exclude more common, alternative causes of abdominal pain. Despite this, the European Society for Vascular Surgery (ESVS) clinical practice guidelines for the management of diseases of mesenteric arteries and veins3 recognizes MALS as the most common cause of single-vessel arterial stenosis, with the potential for significant morbidity. This review aimed to outline the anatomy and pathophysiology of MALS. Evidence pertaining to its clinical presentation, diagnosis, and management is reported. A practical algorithm for the management of suspected MALS is presented.
ANATOMY The MAL is a tough fibrous arch connecting the right and left crura of the diaphragm at the level of the aortic hiatus (T12-L1). It traverses anterior to the aorta and is usually cranial to the celiac artery. The position of the MAL and the origin of the celiac artery vary between individuals. A relatively cranial origin of the celiac artery or caudal insertion of the MAL can lead to extrinsic compression of the proximal celiac artery. In 1971, Lindner 1
2
Goodall et al
Journal of Vascular Surgery ---
and Kemprud4 conducted a fresh autopsy study of 75 specimens and noted significant anatomic variability of the MAL. In 33% of patients, the origin of the celiac artery was at or above the level of the MAL. The variation was predominantly due to caudal level and character of the MAL rather than to cranial origin of the celiac artery. This anatomic phenomenon can lead to compression of the celiac artery. The degree of celiac artery compression is subject to respirational variation. In 1973, Reuter and Bernstein5 placed clips on the free edge of the MAL and demonstrated the tendency for ventral movement of the clips and caudal movement of the celiac artery during deep inspiration on lateral aortography, manifested as a tendency to decrease celiac artery compression during deep inspiration and to increase the compression during expiration. Chronic compression by the MAL can lead to hyperplastic intimal changes of the celiac artery. Histologic studies have demonstrated an abundance of smooth muscle proliferation, abnormal elastic fibers, and disorganized medial and adventitial layers that may advance to cause complete arterial occlusion in patients with MALS.6 Downstream of the stenosis, poststenotic dilation and celiac artery aneurysms can complicate MALS further. The visceral artery aneurysm rate in the general population is reported at between 0.1% and 2%; in MALS, it was reported as 48% in a single-center retrospective cohort of 23 patients.7 Of the 11 patients with visceral artery aneurysms, 73% had aneurysmal disease in the pancreaticoduodenal arcade, 27% in the splenic artery, and 18% in the celiac artery. Furthermore, the proximity of the celiac ganglion to the compressed celiac artery and evidence of symptomatic benefit after interventions targeting the celiac ganglion8 have led to postulations that neuropathic pain is a contributory factor in MALS. The mechanism for this is thought to be compression of the celiac ganglion by the MAL and subsequent overstimulation of pain fibers of the sympathetic nervous system.6
PRESENTATION The true prevalence of MALS is unclear, which is partly due to its variable clinical presentation. There is a tendency toward a female phenotype (4:1), and the median age typically lies between 30 and 50 years.9 Cases have also been reported in pediatric populations.10 Frequently reported symptoms include epigastric pain, nausea, vomiting, weight loss, and postprandial or exercise-induced abdominal pain. Clinical signs may include abdominal bruits (amplified with expiration), epigastric tenderness, and marked weight loss. In a case series of 43 individuals treated surgically for MALS11 (defined in the study as the presence of unexplained chronic abdominal symptoms and angiographic evidence of >50% compression of the proximal celiac
2019
artery), the pretreatment clinical features included abdominal pain in 91% of patients (which was postprandial in 62%, postexertional in 32%, and unprovoked in 33%). In addition, 40% of individuals had weight loss, 30% had nausea, and 47% had audible epigastric bruits. In a retrospective cohort12 of 344 asymptomatic individuals undergoing computed tomography angiography (CTA) before live kidney donation, evidence of celiac artery compression of >50% by the MAL was reported in 3.4% of individuals. Furthermore, in a retrospective database analysis13 of 744 patients in whom CTA was performed for various indications, radiologic evidence of celiac artery compression by the MAL was present in 2.8% of cases. Interestingly, only three patients with radiologic evidence of celiac artery compression presented with symptoms of MALS. This retrospective study probably under-reported the true symptom rate, but an additional explanation for the lack of symptoms in patients with radiologic evidence of MALS may be the development of collateral circulation. Heo et al14 demonstrated collateral circulation in 46% of their cohort of 32 asymptomatic patients with radiologic evidence of MALS. Intriguingly, ska et al15 noted a significantly positive correlation Arazin between the degree of celiac artery stenosis and the presence of collateral circulation (Spearman correlation coefficient ¼ 0.339; P < .001) on CTA. An emerging theme in the literature is the presence of psychiatric comorbidities in a significant proportion of patients with MALS. In a prospective observational analysis16 of 51 patients undergoing surgical intervention for MALS (defined as chronic abdominal pain with radiologic evidence of extrinsic celiac artery compression and altered celiac artery hemodynamics), 28% of patients demonstrated preoperative symptoms consistent with a psychiatric disorder according to criteria from the Diagnostic and Statistical Manual of Mental Disorders (Fourth Edition, Text Revision). Anxiety disorders predominated, a theme that appears consistent.16-18 Pediatric patients also appear vulnerable to the coexistence of MALS and psychiatric disorders. Mak et al18 demonstrated similar pediatric psychosocial profiles (notably a high incidence of anxiety and mood disorders) in patients with MALS to patients with other gastrointestinal disorders resulting in chronic abdominal pain, including inflammatory bowel disease. Reilly et al19 concluded from their 1985 case series with a 9-year mean follow-up that improved surgical outcomes correlated with lack of psychiatric history. Similarly, Skelly et al16 concluded that a preoperative psychiatric diagnosis predicted a lower postsurgical overall quality of life. Analysis of the raw data from the prospective observational analysis of Skelly et al, however, suggests alternative conclusions. Patients with a coexistent psychiatric diagnosis had a significantly lower overall quality of life score preoperatively compared with those without psychiatric diagnoses. Intriguingly,
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
3
-
Fig 1. Diagnostic imaging. A, Duplex ultrasound (DUS) image (in expiration) of the abdominal aorta revealing steep angulation of the celiac axis (arrow). Orientation: cranial end to the right of the image. B, Sagittal threedimensional volume-rendered image of the abdominal aorta demonstrating narrowing and angulation of proximal celiac artery (arrow).
the overall difference in quality of life scores actually was reduced postoperatively from 12.9 points (P ¼ .007) to 11.3 points (P ¼ .01), suggesting a relatively greater improvement in overall quality of life in those with a preexistent psychiatric disorder. A large dropout rate of 44 of a total 95 patients operated on for MALS also limits reliable conclusions from this study.
DIAGNOSIS Diagnosis of MALS typically depends on exclusion of alternative causes of abdominal pain. Indeed, before investigation for MALS, a formal gastroenterology review is advisable to rule out more common explanations for the patients’ symptoms; esophagogastroduodenoscopy, colonoscopy, motility studies, and cross-sectional imaging and relevant hematologic studies should be obtained. The ESVS clinical practice guideline on the management of mesenteric disease3 provides recommendations as how best to investigate patients with suspected chronic mesenteric ischemia. The guideline refers to MALS in the chronic mesenteric ischemia section and recognizes MALS as the most common cause of single mesenteric vessel stenosis. However, the document also states that the symptoms observed in MALS may not be caused by chronic mesenteric ischemia; therefore, the ensuing diagnostic and treatment recommendations in the guideline, which are based predominantly on chronic mesenteric ischemia resulting from multivessel stenotic disease of an atherosclerotic pathophysiologic process, have limited applicability to MALS. To the authors’ knowledge, no other group consensus agreement as to the diagnosis of MALS exists. Unremarkable findings on abdominal ultrasound, computed tomography, and upper gastrointestinal endoscopy are common in patients with MALS. When
clinical suspicion of chronic mesenteric ischemia arises, duplex ultrasound (DUS) is the first-line recommended investigation3 (Fig 1). DUS is advantageous as an initial investigation compared with angiography as it is cheaper and noninvasive, and it does not expose patients to high doses of radiation. Gruber et al20 conducted a retrospective cohort study of 364 patients undergoing DUS of the celiac trunk. Of the six patients with a retrospective diagnosis of MALS (based on chronic abdominal symptoms and angiographic evidence of celiac artery stenosis with extrinsic compression), 100% had celiac trunk deflection angles of >50 degrees compared with 40% in the asymptomatic control group (8/20 patients). Their analysis demonstrated significant differences in expiratory peak systolic flow velocities (PSVs) in the patients with MALS (mean PSV, 425 6 130.1 cm/s) compared with asymptomatic controls (mean PSV, 209.9 6 80.1 cm/s; two-tailed Mann-Whitney U, P ¼ .001). They concluded that a combination of a deflection angle >50 degrees and an expiratory PSV of >350 cm/s confers 83% sensitivity, 100% specificity, and 100% positive predictive value for a diagnosis of MALS in their patient group. Data were obtained from a small sample size (n ¼ 14), however, and the possibility of interobserver and intraequipment variability must also be considered. CTA is an additional noninvasive imaging tool to diagnose arterial occlusion. Three-dimensional images of the mesenteric arteries, the position of the MAL, and imaging able to detect differential diagnoses are rapidly acquired. The ESVS guideline3 states that in patients in whom there is a moderate to high suspicion of chronic mesenteric ischemia, CTA is recommended to map occlusive disease and to detect or to exclude other intra-abdominal disease. CTA features in MALS include focal narrowing of the proximal celiac artery with a characteristic hooked appearance.21 This “hooking” helps
4
Journal of Vascular Surgery
Goodall et al
---
differentiate MALS stenosis from atherosclerotic narrowing. CTA also permits better appreciation of poststenotic dilation and visceral artery aneurysms compared with DUS. On the contrary, changes in vessel caliber and flow velocity with respiration are more easily appreciated with DUS. Magnetic resonance angiography and digital subtraction angiography (DSA) can provide similar appreciation of vessel stenosis as CTA. Angiography also permits appreciation of the degree of collateralization accompanying the celiac artery stenosis. This may be of clinical importance with respect to predicting the patient’s response to treatment. van Petersen et al22 performed a retrospective analysis of 129 patients with MALS (diagnosed as chronic unexplained abdominal pain, radiologic evidence of extrinsic celiac artery compression, and objective evidence of gastric ischemia on tonometry) who underwent decompression of the MAL through retroperitoneal open or endoscopic techniques. The authors demonstrated that individuals with extensive collateral mesenteric circulation (classified as at least one collateral clearly visible on nonselective DSA) are less likely to benefit from MAL release compared with individuals with no or less extensive collateralization (ie, no visible collaterals or collaterals visible on selective DSA but not visible on nonselective DSA). Magnetic resonance angiography, DSA, and CTA should be performed in inspiration and expiration to demonstrate the changes in celiac artery compression with the phases of respiration. Interestingly, a convincing correlation between degree of angiographic stenosis and likelihood of being symptomatic from MALS is lacking. Stenosis of >50% of the celiac artery produced symptoms in only 1 of 8 patients in a retrospective observational study of >1000 individuals who underwent CTA.23 Gastric exercise tonometry (GET) is reported to be 76% sensitive and 92% specific for the diagnosis of intestinal ischemia.24,25 A positive GET study results from a rising intraluminal partial pressure of carbon dioxide from anaerobic respiration. In a prospective cohort study, Mensink et al26 demonstrated positive GET results in 29 of 43 patients with abdominal pain and significant celiac artery compression (stenosis of >70% visible on DSA). Patients then underwent MAL release (22 patients underwent MAL release alone and 7 patients received MAL release with celiac artery reconstruction). At a median follow-up of 39 months, those who were symptom free (83%) had normal findings on GET, whereas abnormal GET results persisted in 25% of patients with ongoing symptoms (P < .001). They concluded that this suggested that MALS was an ischemic syndrome and that surgical intervention can effectively treat the ischemic phenomenon, which would in turn be manifested as resolution of symptoms. However, the remaining 13 symptomatic patients with positive DSA and negative GET results did not receive surgical MAL release,
2019
which limits important comparisons. Moreover, despite its apparently high diagnostic accuracy, GET is not ubiquitous and is a complicated and time-intense procedure. The contribution of compression of the celiac plexusdwhich conveys foregut visceral afferent pain sensationdby the MAL has also been suggested by some as a diagnostic target in MALS.27,28 Weber et al27 performed preoperative, temporary percutaneous celiac plexus block using a local anesthetic agent in four patients with radiologic evidence of MALS with atypical symptoms; 100% of these patients described symptom relief after the block, and all reported symptom relief after subsequent laparoscopic decompression. Indeed, a positive response to a diagnostic celiac plexus block may predict good response to surgical decompression and celiac ganglionectomy; however, quality evidence to support this statement is lacking. Moreover, evidence demonstrating the differential benefits of celiac ganglion block in individuals with chronic unexplained abdominal pain and radiologic evidence of MALS, with vs without GET results positive for ischemia, is lacking. An understanding of the differing contribution of the celiac plexus to symptoms across the MALS disease spectrum represents an area for future research to improve targeted therapy.
MANAGEMENT Interventions for MALS aim to address the hypothesized pathophysiologic mechanisms: decompression of the MAL’s constriction of the celiac artery, with or without celiac ganglionectomy to target the neuropathic component to the pain. Fig 2 demonstrates a suggested diagnosis and treatment algorithm for patients with suspected MALS based on review of the currently available literature. Decompression of the celiac artery was traditionally achieved through an open approach, in which a chevron or upper midline laparotomy permits identification of the MAL and celiac artery. The compressive band is then divided, along with division and wide excision of the celiac ganglion (ganglionectomy), and the proximal celiac artery is completely exposed. Celiac ganglionectomy rather than simple neurolysis is recommended as a means of addressing the neuropathic pain associated with MALS. Recent years, however, have seen a trend toward laparoscopic intervention to decompress the celiac artery. Endovascular intervention alone does not address the extrinsic compression of the celiac artery and has subsequently proven ineffective as an isolated treatment of MALS.9 Persistent stenosis of the celiac artery after decompression may be appreciated with intraoperative handheld Doppler assessment, angiography, or DUS. This can be addressed with arterial reconstruction, examples of which include an aortoceliac bypass or a celiac artery patch angioplasty. Conversion from laparoscopic to
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
5
-
Fig 2. Median arcuate ligament syndrome (MALS) diagnosis and management. Flow chart demonstrating suggested diagnostic workup and management for patients with MALS. CTA, Computed tomography angiography; DSA, digital subtraction angiography; MAL, median arcuate ligament; MRA, magnetic resonance angiography.
open surgery is typically required for vascular reconstruction. Percutaneous transluminal angioplasty with or without stenting provides an adjunctive endovascular approach to revascularization of a persistent stenosis after MAL release. Jiminez et al29 performed a review of studies reporting on outcomes of surgical interventions for MALS. Twenty studies reporting data from 400 patients undergoing surgical intervention for MALS were included; 279 underwent open MAL division, and 121 received laparoscopic division. Follow-up duration ranged from 10 to 229 months for the open group and 6 to 44 months for the laparoscopic group. The majority of included studies reported data on fewer than 20 patients, with a followup of <3 years. Overall, 85% of patients reported immediate postoperative symptom relief (open group, 78%; laparoscopic group, 96%). Late recurrence rates were 6.8% for patients treated with open MAL division and
5.7% for patients treated laparoscopically; 9.1% of laparoscopic procedures were converted to open surgery because of bleeding. Quality of life outcomes and comparisons of adverse event data were lacking; however, the study states that no procedure-related or early perioperative deaths were reported. Only one of the studies30 included in the review directly compared open MAL release and ganglionectomy (n ¼ 6) with laparoscopic MAL release and ganglionectomy (n ¼ 8) in a cohort of patients with chronic unexplained abdominal pain and radiologic evidence of extrinsic compression of the MAL. The authors concluded that both procedures can be safely performed with minimal morbidity. They noted significant differences only for the length of hospital stay (laparoscopic group, 2.3 days; open group, 7.0 days; P # .05) and time to feeding (open group, 2.8 days; laparoscopic group, 1.0 days; P # .05), both of which were better in the laparoscopic
6
Journal of Vascular Surgery
Goodall et al
---
group. A small sample size (14 patients) and short median follow-up duration (14.0 months) limit conclusions from this study. Moreover, two of the patients in the laparoscopic group required conversion to open surgery because of intraoperative bleeding. Endoscopic retroperitoneal approaches to MAL release have also been reported. In a case series of 46 individuals with a diagnosis of MALS31 (based on positive symptoms, angiographic evidence of celiac artery compression, and GET results positive for ischemia), 89% of patients reported either symptom resolution or significant improvement at a median follow-up of 20 months. Only one patient required conversion to laparotomy (because of bleeding from the suprarenal artery), and pneumothorax occurred in three individuals. No other complications were reported, and the mean hospital stay was 5.6 days. Ho et al11 compared outcomes of surgical intervention (laparoscopic [n ¼ 38] or open [n ¼ 5] MAL release) with nonoperative management for MALS. A diagnosis of MALS was made on the basis of symptoms of chronic abdominal pain and radiologically confirmed extrinsic compression of the celiac artery (GET was not part of the diagnostic workup). They reported symptom resolution or improvement in 95% of patients in the surgical group (n ¼ 43) compared with 33% in the nonoperative group (n ¼ 24) after a retrospective review. However, group differences limit reliable comparisons. Notable differences included more patients with celiac artery stenosis >70% (surgical group, 62%; nonoperative group, 36%) and fewer patients with unprovoked abdominal pain (surgical group, 33%; nonoperative group, 64%) in the surgical group compared with the nonoperative group. Robot-assisted MAL release and celiac ganglionectomy represents an emerging treatment modality for individuals with MALS. Do et al32 found that laparoscopic MAL release had significantly shorter operative times than robot-assisted laparoscopic release but concluded that both are safe and effective interventions in their retrospective cohort of 16 patients with unexplained chronic abdominal symptoms and celiac artery compression. Direct, randomized comparisons of MAL release with and without arterial revascularization (in the form of celiac artery reconstruction or percutaneous transluminal angioplasty) are lacking. Schweizer et al33 presented a retrospective case series of eight pediatric patients with MALS (diagnosis based on symptoms of chronic abdominal pain and an audible epigastric bruit) who underwent surgical MAL release without any form of arterial revascularization, and all were symptom free at the end of follow-up (follow-up range, 3-18 years). Furthermore, van Petersen et al22 performed MAL release through an endoscopic retroperitoneal approach in 46 patients with symptoms and GET evidence of ischemia. In 36 of these patients, arterial reconstruction or endovascular revascularization was not performed. At a median follow-up of 20 months, 89% of all patients were free of
2019
symptoms or showed significant symptomatic improvement. On the contrary, a retrospective cohort34 of eight adult individuals with MALS treated with open MAL release and celiac ganglionectomy without arterial revascularization had a 100% symptom recurrence rate at the end of follow-up (mean, 19.1 years). Predicting the patients in whom arterial reconstruction would offer benefit represents an ongoing challenge in the management of MALS. Moving forward, the published interventional research suggests that clinical equipoise likely exists to permit direct, prospective, perhaps even randomized comparisons of open, laparoscopic, endoscopic retroperitoneal, and robot-assisted decompression of the celiac artery for treatment of MALS. Given the relative rarity of MALS presentation, a multicenter collaborative trial would likely be appropriate to obtain adequate patient numbers. Prospective studies might consider including targeted psychiatric interventions as an adjunct to surgical management, and the diagnostic value of preoperative percutaneous celiac plexus block represents an additional area for investigation. Emphasis should be placed on better classification of individuals likely to respond to surgical intervention and clarification of the roles of celiac ganglionectomy and arterial revascularization in disease management. Robust comparisons of length of hospital stay, adverse events, reintervention rates, persistence of celiac artery stenosis, and, importantly, long-term symptom relief resulting from each of the surgical approaches should be presented.
CONCLUSIONS The available evidence is highly suggestive that MALS exists. Despite no definitive group consensus agreement as to the diagnostic criteria or management of MALS, patient presentation and radiologic signs appear generally consistent across the literature. Moreover, recent procedural studies agree that surgical intervention can treat this controversial but debilitating condition. Currently, however, inadequate long-term (>5 years) follow-up data limit assumptions as to whether surgery is effective for treatment of MALS. Consensus as to the optimal surgical approach to management is also lacking. Despite this, an increased awareness of MALS would permit earlier consideration and investigation of the syndrome as part of a diagnostic workup for patients with symptoms of abdominal pain and weight loss not attributable to more common conditions.
AUTHOR CONTRIBUTIONS Conception and design: RG, BL, SO, AD Analysis and interpretation: RG, SO, ME, TL, AD Data collection: Not applicable Writing the article: RG, BL, SO Critical revision of the article: RG, BL, SO, ME, TL, AD Final approval of the article: RG, BL, SO, ME, TL, AD
Journal of Vascular Surgery Volume
-,
Number
Goodall et al
7
-
Statistical analysis: Not applicable Obtained funding: Not applicable Overall responsibility: AD
REFERENCES 1. Harjola PT. A rare obstruction of the celiac artery. Ann Chir Gynaecol Fenn 1963;52:547-50. 2. Dunbar JD, Molnar W, Beman FF, Marable SA. Compression of the celiac trunk and abdominal angina. Am J Roentgenol Radium Ther Nucl Med 1965;95:731-44. 3. Bjork M, Koelemay M, Acosta S, Bastos Goncalves F, Kölbel T, Kolkman JJ, et al. Management of the diseases of mesenteric arteries and veins. Eur J Vasc Endovasc Surg 2017;53: 460-510. 4. Lindner HH, Kemprud E. A clinicoanatomical study of the arcuate ligament of the diaphragm. Arch Surg 1971;103: 600-5. 5. Reuter SR, Bernstein EF. The anatomic basis for respiratory variation in median arcuate ligament compression of the celiac artery. Surgery 1973;73:381-5. 6. Bech FR. Celiac artery compression syndromes. Surg Clin North Am 1997;77:409-24. 7. Nasr LA, Faraj WG, Al-Kutoubi A, Hamady M, Khalifeh M, Hallal A, et al. Median arcuate ligament syndrome: a singlecenter experience with 23 patients. Cardiovasc Intervent Radiol 2017;40:664-70. 8. Sultan S, Niamh H. PS160. Management of median arcuate ligament syndrome (MALS) with decompression and coeliac ganglion sympathectomy (CGS) for chronic mesenteric ischaemia (CMI). Procedural, clinical and enduring results with quality-adjusted time spent without symptoms of disease and toxicity of treatment (Q-TWiST). J Vasc Surg 2010;51:62S. 9. Kim EN, Lamb K, Relles D, Moudgill N, DiMuzio PJ, Eisenberg JA. Median arcuate ligament syndromedreview of this rare disease. JAMA Surg 2016;151:471-7. 10. Scholbach T. Celiac artery compression syndrome in children, adolescents, and young adults: clinical and color duplex sonographic features in a series of 59 cases. J Ultrasound Med 2006;25:299-305. 11. Ho KK, Walker P, Smithers BM, Foster W, Nathanson L, O’Rourke N, et al. Outcome predictors in median arcuate ligament syndrome. J Vasc Surg 2017;65:1745-52. 12. Petnys A, Puech-Leão P, Zerati AE, Ritti-Dias RM, Nahas WC, Neto ED, et al. Prevalence of signs of celiac axis compression by the median arcuate ligament on computed tomography angiography in asymptomatic patients. J Vasc Surg 2018;68: 1782-7. 13. Gümüs H, Gümüs M, Tekbas G, Önder H, Ekici F, Cetinçakmak MG, et al. Clinical and multidetector computed tomography findings of patients with median arcuate ligament syndrome. Clin Imaging 2012;36:522-5. 14. Heo S, Kim HJ, Kim B, Lee JH, Kim J, Kim JK. Clinical impact of collateral circulation in patients with median arcuate ligament syndrome. Diagn Interv Radiol 2018;24:181-6. ska A, Polguj M, Wojciechowski A, Trębin ski q, 15. Arazin czyk L. Median arcuate ligament syndrome: predictor Stefan of ischemic complications? Clin Anat 2016;29:1025-30. 16. Skelly C, Stiles-Shields C, Mak GZ, Speaker CR, Lorenz J, Anitescu M, et al. The impact of psychiatric comorbidities on patient-reported surgical outcomes in adults treated for the median arcuate ligament syndrome. J Vasc Surg 2018;68: 1414-21. 17. Columbo J, Trus T, Nolan B, Goodney P, Rzucidlo E, Powell R, et al. Contemporary management of median arcuate
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
ligament syndrome provides early symptom improvement. J Vasc Surg 2015;62:151-6. Mak G, Speaker C, Anderson K, Stiles-Shields C, Lorenz J, Drossos T, et al. Median arcuate ligament syndrome in the pediatric population. J Pediatr Surg 2013;48:2261-70. Reilly LM, Ammar AD, Stoney RJ, Ehrenfeld WK. Late results following operative repair for celiac artery compression syndrome. J Vasc Surg 1985;2:79-91. Gruber H, Loizides A, Peer S, Gruber I. Ultrasound of the median arcuate ligament syndrome: a new approach to diagnosis. Med Ultrason 2012;14:5-9. Horton KM, Talamini MA, Fishman EK. Median arcuate ligament syndrome: evaluation with CT angiography. Radiographics 2005;25:1177-82. van Petersen AS, Kolkman JJ, Gerrits DG, van der Palen J, Zeebregts CJ, Geelgerken RH, et al. Clinical significance of mesenteric arterial collateral circulation in patients with celiac artery compression syndrome. J Vasc Surg 2017;65: 1366-74. Baskan O, Kaya E, Gungoren FZ, Erol C. Compression of the celiac artery by the median arcuate ligament: multidetector computed tomography findings and characteristics. Can Assoc Radiol J 2015;66:272-6. Otte JA, Geelkerken RH, Oostveen E, Mensink PB, Huisman AB, Kolkman JJ. Clinical impact of gastric exercise tonometry on diagnosis and management of chronic gastrointestinal ischemia. Clin Gastroenterol Hepatol 2005;3: 660-6. Sana A, Vergouwe Y, van Noord D, Moons LM, Pattynama PM, Verhagen HJ, et al. Radiological imaging and gastrointestinal tonometry add value in diagnosis of chronic gastrointestinal ischemia. Clin Gastroenterol Hepatol 2011;9:234-41. Mensink PB, van Petersen AS, Kolkman JJ, Otte JA, Huisman AB, Geelkerken RH. Gastric exercise tonometry: the key investigation in patients with suspected celiac artery compression syndrome. J Vasc Surg 2006;44:277-81. Weber JM, Boules M, Fong K, Abraham B, Bena J, El-Hayek K, et al. Median arcuate ligament syndrome is not a vascular disease. Ann Vasc Surg 2016;30:22-7. Gloviczki P, Duncan AA. Treatment of celiac artery compression syndrome: does it really exist? Perspect Vasc Surg Endovasc Ther 2007;19:259-63. Jiminez JC, Harlander-Locke M, Dutson EP. Open and laparoscopic treatment of median arcuate ligament syndrome. J Vasc Surg 2012;56:869-73. Tulloch AW, Jiminez JC, Lawrence PF, Dutson EP, Moore WS, Rigberg DA, et al. Laparoscopic versus open celiac ganglionectomy in patients with median arcuate ligament syndrome. J Vasc Surg 2010;52:1283-9. van Petersen AS, Vriens BH, Huisman AB, Kolkman JJ, Geelkerken RH. Retroperitoneal endoscopic release in the management of celiac artery compression syndrome. J Vasc Surg 2009;50:140-7. Do MV, Smith TA, Bazan HA, Sternbergh WC 3rd, Abbas AE, Richardson WS. Laparoscopic versus robot-assisted surgery for median arcuate ligament syndrome. Surg Endosc 2013;27:4060-6. Schweizer P, Berger S, Schweizer M, Schaefer J, Beck O. Arcuate ligament vascular compression syndrome in infants and children. J Pediatr Surg 2005;40:1616-22. Geelkerken RH, Van Bockel JH, De Roos WK, Hermans J. Br J Surg 1990;77:807-9.
Submitted Jul 29, 2019; accepted Nov 3, 2019.