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Dec 9, 2014 - 2015 Hans Huber Publishers, Hogrefe AG, Bern. Introduction. The celiac artery compression syn- drome (CACS) is an abdominal.
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A. Klimas et al.: Celiac artery compression syndrome DOI 10.1024/0301 – 1526/a000446

Original communication 305

Laparoscopic treatment of celiac artery compression syndrome in children and adolescents Annegret Klimas1, Andreas Lemmer2, Hendrik Bergert3, Michael Brodhun4, Thomas Scholbach5, and Kay Großer1 1

Department of Pediatric Surgery and Pediatric Urology, HELIOS Klinikum Erfurt, Germany Department of Pediatrics, HELIOS Klinikum Erfurt, Germany 3 Department of Vascular Surgery, HELIOS Klinikum Erfurt, Germany 4 Department of Pathology, HELIOS Klinikum Erfurt, Germany
 5 Department of Radiology, Ultrasound Practice Leipzig, Germany
 2

Summary: Background: The celiac artery compression syn-

drome (CACS) is a rarely diagnosed disorder, which is characterized by chronic abdominal pain and vegetative symptoms. The role of surgical treatment in celiac artery decompression has been discussed controversially by numerous authors. After first casuistic descriptions of a laparoscopic treatment in adults we established this novel minimally invasive procedure for treatment in children and adolescents. Patients and methods: Between 2005 and 2014 we operated 58 patients (47 female, 11 male) from 7 to 25 years who had been diagnosed with celiac artery compression. The patients presented with severe chronic abdominal pain, vegetative symptoms and a reduced quality of life. Doppler sonography showed an increased blood flow velocity of the celiac artery with maximum of 190 – 450 cm/s (mean 259 cm/s).MR angiography demonstrated a characteristic hook-shaped appearance of the celiac artery with severe localized compression.

Results: All patients underwent laparoscopic decompression of the celiac artery. We observed complications in 3 patients (5,2 %). Postoperatively all patients (100 %) were immediately free of abdominal pain. Doppler sonography showed a marked reduction in celiac blood flow velocity to 70 – 190 cm/s postoperatively (mean 178 cm/s). A return of vessel diameters to normal dimensions was documented by postoperative MR angiography. During a median follow up of 62 months we observed a recurrence of the celiac artery compression in 4 patients (6,9 %). Conclusions: Laparoscopic treatment of celiac artery compression syndrome offers a novel, safe, reliable and, compared to open surgery, less invasive approach. The surgical treatment is indicated in patients with characteristic symptoms and typical findings at Doppler sonography and MRA after exclusion of other abdominal pathologies. The work-up of chronic abdominal pain in children and adolescents should include a color Doppler sonography to look for celiac artery compression.

Key words: Chronic abdominal pain, compression of the celiac artery, median arcuate ligament syndrome, laparoscopic decompression of the celiac artery, Dunbar syndrome

Introduction The celiac artery compression syndrome (CACS) is an abdominal neurovascular pain syndrome with accompanying vegetative symptoms. It is caused by an external compression of the celiac artery at its origin by the median arcuate ligament. The median arcuate ligament is a fibrous arch, formed at the base of the diaphragm where the left and right diaphragmatic crura join near the 12th thoracic vertebra. It makes up the ventral border of the aortic hiatus. Normally, the ligament lies above the branch point of the celiac artery. Between the arcuate ligament and the celiac artery lies the celiac plexus.

Changes of the spatial relationships of these structures may cause a compression of the celiac plexus and the underlying celiac artery, mainly due to a descensus of the diaphragm in patients with prominent lumbar lordosis or after periods of accelerated growth in children and adolescents. This compression is increased by expiration and decreases with inspiration [1, 2]. In up to 25 % of normal individuals, the median arcuate ligament passes in front of the celiac artery, compressing the celiac artery and the celiac plexus. In some of these individuals, this compression is pathologic and leads to the celiac artery compression syndrome.

Since the first reports of this entity by Harjola 1963 [3] and Dunbar 1965 [4] the controversy about the causal link to patients’ complaints has never stopped. The origin of pain seems to be the chronic respirationdependent mechanical irritation of the celiac plexus nerve fibers and not the compression of the vessel. Purely hemodynamic explanations for the symptoms fail to explain the well documented fact, that an abundant collateralization develops very early and thus bypasses the compression site. The demonstration of the vascular stenosis itself serves only as a diagnostic marker. It must not be taken for the direct cause of complaints [5].

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Figure 1: Dopplersonographic image of the celiac artery with color aliasing. The arrow pointed to the narrowed proximal celiac artery at the take-off from the aorta.

The incidence of this vaguely characterized disease is not known. In children and adolescents with abdominal

pain a prevalence of 1,5 % was found [5]. Typical symptoms are chronic or recurring and often stabbing epigastric pain attacks with accompanying vegetative symptoms encompassing nausea, dizziness, tachycardia, diarrhea, weight loss and sweating [6]. These rather unspecific complaints may last for several hours and very

often reduce the quality of life severely. The diagnosis can be made straightforwardly by color Doppler sonographic examination of the celiac artery in in- and expiration. A significant acceleration of flow and turbulences lead to the diagnosis (Fig. 1). Flow velocity usually rises with expiration and is less increased during inspiration. If there is no change of the flow velocity we speak of fixed stenosis, like a classical intrinsic stenosis of the vessel [7]. In many cases compression of the celiac artery can be readily demonstrated by MR-angiography (MRA) (Fig. 2). Here, a typical hook-like downward displacement followed by a dilatation of the celiac artery are characteristic findings [8]. In 30 – 50 % of all incidentally found cases of celiac artery compression no symptoms can be found [9]. This can be explained by the individual variations of the celiac plexus, its size, shape and position in relation to the arcuate ligament. On the other hand, many other diseases may cause similar symptoms. Thus, other relevant abdominal pathologies must be ruled out before a surgical intervention is considered (Tab. I). The surgical

Table I: Main differential diagnoses of celiac artery compression syndrome Abdominal pathologies – Gastritis/gastroduodenitis – Gastroesophageal reflux – Cholelithiasis – Pancreatitis – Liver diseases – Inflammatory bowel disease – Food intolerances or non allergic food hypersensitivity – Kidney diseases/urological pathologies

Figure 2: High grade stenosis and a typical hook-like downward displacement followed by a dilatation of the celiac artery are characteristic findings in MR angiography.

Thoracic disorders – Pericarditis – Pleuritis – Esophagitis Psychic or neurological disorders – Chronic depression – Chronic fatigue syndrome

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treatment (Fig. 3) consists of division of the median arcuate ligament and the fibers of the celiac plexus [2]. In case of secondary fixed stenosis in adults, balloon angioplasty can be discussed after decompression of the artery [10]. Even surgical treatment is not uncontroversial. The primary failure rate of open surgery is reported to be 25 % or higher [11] and the recurrence rate in adults 40 % [12]. The open surgical approach is a relatively invasive technique, due to the anatomical position of celiac artery. Roayaie 2000 [13] and Dordoni 2002 [14] were the first to publish case reports of less invasive laparoscopic treatments. Since 2005 we have established our own minimally invasive laparoscopic technique resembling the technique described by Roayaie and Dordoni.

Patients and methods Overall 68 patients (most of them other regions) with suspected CACS were referred to our clinic to assess the indication for surgery. In 58 of these patients (85,3 %) we decided to treat surgically. 10 Patients (14,7 %) were not operated but remained under outpatient control. They did not fulfill the criteria for CACS and were not included in the current study. We performed a laparoscopic decompression of the celiac artery in 58 patients (47 female, 11 male) between 2005 and 2014. Their mean age was 16,6 years (7 – 25 y). All 58 patients (100%) suffered from chronic and recurrent epigastric pain and complained about severe restriction of their quality of life. Two patients (3,45 %) had a pain intensity of 10, 12 patients (20,7 %) of 9, 16 patients (27,6 %) of 8, 15 patients (25,9 %) of 7 and 13 patients (22,4 %) of 6 on a 10-grade individual visual pain scale.

Figure 3: Median arcuate ligament makes up the ventral border of the aortic hiatus. It can cause a compression of celiac artery and a chronic irritation of the underlying celiac plexus. Principle of operation technique - aortic hiatus before and after the decompression of the celiac artery [31].

Additional vegetative symptoms were prevalent: in 45 % general weakness, in 43 % nausea, in 37 % dizziness, in 27 % bouts of sweating, in 27 % weight loss, in 23 % diarrhea and tachycardia in 20 %.

The mean duration of symptoms was 29 months (range 3 – 72 months). In all patients color Doppler sonography was performed and revealed maximum flow velocities of 190 – 450  cm/s (mean 259  cm/s). The MR-angiography showed a typi-

Table II: Preoperative work-up Routine diagnostics – Laboratory work-up – Ultrasound/color Doppler sonography – MR angiography – Gastroscopy – Exclusion of food intolerances and allergies – Stool examinations: calprotectin, infectious agents (incl. parasites) Optionally – Cranial MRI – Colonoscopy – Cardiological check up – Gynecological examination – Psychological check up

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done under general anesthesia and a simultaneous peridural anesthesia. The patients placed in a supine position. Five trocars were inserted: supraumbilically and in the left upper quadrant with 10 mm diameter, central abdomen, right upper quadrant and left middle abdomen with 5 mm diameter. Initially, a diagnostic laparoscopy was made to exclude relevant differential diagnoses. The same access like in fundoplication was used. After retraction of the liver the flaccid part of gastrohepatic omentum was dissected. The fascia of the diaphragm was opened directly in front of the pulsating aorta. Next, the muscles of the diaphragmatic crura were dissected until the ventral surface of the aorta proximal to the arcuate ligament was revealed. Then, under continual traction, the broad bands of connective tissue of the arcuate ligament were exposed and divided step by step with the monopolar hook. Quite often all three branches of the celiac artery were surrounded by the connective tissue of the ligament and thus had to be exposed very cautiously. After complete division of the ligament a very careful dissection of the weblike fibers of the celiac plexus overlying the vessel was performed (Fig. 4 and 5). If the celiac artery was freed circumferentially, an erection of the vessel was observed. Finally a wound drainage was placed. Follow up program included postoperative MRA and Doppler sonography. Long-term controls via MRA or Doppler sonography were not performed. Recurring clinical complaints are the only criterion for relapse. In the case of recurrence of symptoms the patients were advised to contact us. Then we repeated complete diagnostic work-up. On the other hand we wanted to avoid psychic sensitization to relapse.

Follow-up data for the current retrospective study was acquired by mail questionnaire.

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Figure 4: Hypertrophic median arcuate ligament (MAL). The arrow pointed to the mobilised ligament. The ventral wall of the aorta is revealed proximal of the take-off of celiac artery.

Figure 5: Ventral wall of the aorta and celiac artery after complete decompression.

cal hook-like displacement and stenosis of the celiac artery in varying degrees (from a slight narrowing to complete obstruction) in all 58 patients (100 %). To rule out other pathologies we made the following examinations (Tab. II). In 58 patients a laparoscopic decompression of the celiac artery was

Results The duration of the operation was 90 to 180 minutes (mean 143,3 minutes, median 150 minutes, SD ± 25,12). During initial diagnostic laparoscopy no other relevant diagnoses were found. In two cases (3,4 %) we converted to open surgical technique because bleeding occurred, once from the celiac artery and once from a branch vessel of the aorta. Altogether, we observed two major (3,4 %) and one minor (1,7 %) complication (for a total of 5,1 % complications). Major complications were in one case a lesion of the abdominal esophagus and in the other case a lesion of the celiac artery with bleeding. The esophageal leak was closed successfully by an endoscopic stent implantation for 20 days. In the other case it was necessary to reconstruct the celiac artery by autologous saphenous vein grafting. A minor complication was the case of an infected postoperative chylous cyst (diameter 10 cm) at the operative site. It was drained successfully. The median arcuate ligament was found to vary between rather narrow bands and broad connective tissue plates engulfing the celiac artery and its branches. These plates were quite often very adherent to the vessel wall due to fibers sprouting from the celiac plexus and intermingling with the connective tissue fibers. In these cases dissection was more difficult. If possible, histologic specimens from these fibrous ligament structures were taken. They showed fibrosis of the ligament with enclosed hypertrophied nerve fascicles, neuroma-like proliferations of Schwann

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cells and an immigration of small plexus fibres as well as focal vascular changes (Fig. 6 and 7). All 58 patients (100 %) were free of symptoms immediately after the operation. The mean duration of their hospital stay was 7 days. Prior to dismissal, a Doppler ultrasound exam and a MR angiography was done in all patients. In Doppler sonography we found a significant reduction of the flow velocity in the celiac artery from preoperative values of 190 – 450 cm/s (mean 259 cm/s) to 70 – 190  cm/s postoperatively (mean 178 cm/s). The MR angiography demonstrated clearly a regression of the stenotic narrowing and a disappearance of the typical preoperative hook-shaped contour of the celiac artery. Not rarely a persistent stenosis of the artery was seen, despite complete decompression. This was regarded as a secondary or intrinsic stenosis. During follow-up (mean 62 months; range 4 – 126 months) 54 of the 58 patients remained symptom-free (93.1 %). Four (6.89 %) developed a recurrence of symptoms after 6 – 12 months (mean 8 months). Two of them (3,4 %) underwent laparoscopic redo-decompression of celiac artery, once with conversion. In one case (1,7 %) an open technique was chosen since already at the first operation a conversion had been necessary. All three patients remained symptom free during follow–up (mean 25,3 months; range 12 – 36 months). The fourth patient has not been operated yet but is being controlled as an outpatient.

Discussion The syndrome of celiac artery compression is still being debated, both with respect to its pathologic anatomy and the optimal treatment. The true prevalence of this disease is un-

known. The prevalence in our cohort was 85,3 %. This relatively high number is explained by the preselection of our patients. Previously published data show a prevalence of 1,5 % in children and adolescents with abdominal pain [5]. The syndrome mainly affects female individuals. The lower insertion of the diaphragm in women is thought to cause this gender preference [6]. Another plausible explanation is the more pronounced lordosis in women as a result of their deeper and wider pelvis. The correct diagnosis is often missed due to the unspecific complaints. Most of the patients report an odyssey to many specialists while their suffering is dominated by recurrent upper abdominal pain. Many children cannot attend school. They avoid physical or social activities. Work-up of chronic abdominal pain in children and adolescents should include Doppler sonography for exclusion of celiac artery compression syndrome. This diagnostic tool is a reasonable screening test for patients with suspected CACS. It is noninvasive and easily feasible. Furthermore Doppler sonography can clearly help to decide whether the patient needs surgical therapy [15, 16]. The diagnosis of CACS can be made straightforwardly by color Doppler sonographic examination of the celiac artery in in- and expiration [7]. Criteria for diagnosing CACS are different in various publications. Peak systolic velocity (PSV) ranged from 200 – 320cm/s, End diastolic velocity (EDV) from 55 – 100 cm/s [17, 18, 19]. AbuRahma et al. define PSV 200 cm/s as only a moderate stenosis. We operated three of our patients with PSV  280

Figure 6: Biopsy of the median arcuate ligament (Goldner stain): fibrosis of ligament structures and scar is green stained.

a a b

b

b

Figure 7: Biopsy of the median arcuate ligament (S100 stain): hypertrophic nerve fibers with neuroma-like proliferation (a = thick dark red fibers), immigration of small plexus fibers (b = thin dark red fibers) into the ligament.

cm/s and only minimal narrowing of the artery without hook-shape in MRA. All these patients were free of symptoms after surgery. The decision for surgical treatment was not simple and finally determined by the degree of suffering after a period of observation of 3 – 6 months. In our opinion these indications are justified by the lacking correlation between symptom severity and the degree of stenosis.

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Table III: Results of the decompression of the celiac artery in the literature (Ped = pediatric patients, Ad = adult patients, Lap = laparoscopic sugery, Open = open surgery, Rob = robotic surgery) Author Ignashov et al. 2004 [15] Joyce et al. 2013 [20] Mak et al. 2013 [22] Own results Sultan et al. 2013 [23] Do et al. 2013 [24] El Hayek et al. 2013 [25] Berard et al. 2012 [30] Tulloch et al. 2010 [29] Baccari et al. 2009 [26] Grotemeyer et al. 2009 [27] Van Petersen et al. 2009 [28]

Patients 97 6 46 58 11 16 14 11 14 16 18 46

After sonographic diagnosis is established, further evaluation and confirmation can be obtained via angiography or MR angiography to investigate the anatomy of the celiac artery. We recommend MR angiography in children and adolescents as a less invasive technique. The typical findings of focal narrowing of the proximal celiac artery with poststenotic dilatation and the hook-shaped configuration may confirm the diagnosis. The hookshaped contour of the celiac artery is most characteristic and may help to distinguish it from other causes of celiac artery stenosis. MR angiography is an excellent alternative to a catheter angiography, especially in a pediatric population [8]. The indication for surgical treatment cannot be assessed without a thorough search for other relevant diseases of abdominal (intestinal, liver, renal and splenic disorders), thoracic (pleuritis, pericarditis) and eventually also cerebral and neurological disorders (Tab. I). Some patients are often quite sensitive and psychologically unstable. Then a psychiatric work-up is deemed necessary to evaluate the interplay of chronic organic pain and psychic reaction [20].

Ped Ped Ped Ped Ad Ad Ad Ad Ad Ad Ad Ad

Operation

Symptom free n

Follow up %

Open Lap Lap Lap Lap 12 Lap/4 Rob Lap Lap 8 Lap/6 Open Lap Open Lap

87 6 31 54 9 8/2 13 10 5/2 14 15 41

89,7 100 67 93,1 81,8 67/50 92,8 91 62/50 87,5 73,3 89,1

In accordance with Reilly [21] we observed a lacking correlation of symptom severity and the degree of stenosis in Doppler sonography as well as MR angiography. We regard this disease as a purely neural affection. The depictable narrowing and deformation of the celiac artery is to us merely an epiphenomenon pointing to the compression of the celiac plexus nerve fibers situated right onto the vessel and under the median arcuate ligament. The constriction and chronic irritation of the celiac plexus seems to be responsible for the many vegetative symptoms like tachycardia, dizziness, fainting, diarrhea or sweating. Histologic findings regularly demonstrate fibrosis of the ligamentous structures with an immigration of small plexus fibers as well as a hypertrophy and neuroma-like proliferation of nervous fibers. Intraoperatively, a tight adhesion of the arcuate ligament to the celiac artery is found due to the sprouting of plexus fibers into the ligament. We could’nt find an ischemic explanation for symptoms, since in all cases of severe compression abundant pancreatico-duodenal collaterals could be found. Despite this, a secondary intrinsic stenosis

can develop over time, comparable to the May-Thurner-syndrome, with hyperplasia of intimal layer and fibrosis of the vessel wall. The decision to operate is debated critically among many authors because of a high rate of primarily uncontrollable complaints [11] and many recurrences [12]. Diagnostic accuracy in our preselected cohort was 100% since other underlying diseases were excluded and criteria for operation were assured. That emphasizes that diagnosis of CACS only can be made after a complete diagnostic work-up (Tab. II). CACS is a diagnosis of exclusion. Surgical success rate in adults with fixed stenosis is quoted to be only 70 – 80% [11]. Open surgical techniques are relatively invasive. They require a transverse or median laparotomy. We developed a minimal invasive approach following Roayaie’s and Dordoni’s technique. In addition to the general assets such as pain reduction, shorter hospital stay and faster realimentation, we see an advantage in the image magnification effect by optics. That allows a subtle and gentle dissection of the nerve fibers and the vessel wall. The draw-

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back is the need to convert to an open technique in case of uncontrollable bleeding. We reserve four blood units for each patient and have a vascular surgical telephone stand-by. We recommend the following indications for operating children and adolescents with celiac artery compression: 1. Characteristic symptoms leading to a relevant decline in the quality of life 2. Doppler sonographic finding of a relevant compression with flow acceleration to over 200 cm/s depending upon different phases of breathing, mostly decreasing in inspiration 3. MRA confirmation of celiac artery compression 4. All other relevant diseases having been ruled out (Tab. I) The surgeon should be experienced in minimal-invasive techniques. The exact recognition and the safe identification of anatomical structures are subject to a learning curve. In many patients we found a wide and thick arcuate ligament overlying the celiac artery like a roof and circumferentially including the branches of the celiac artery. Particularly in these cases we needed a learning curve. Here it was crucial to differentiate clearly between vascular tissue and the fibrous connective tissue of the ligament. It was very important to perform the dissection carefully and gently to avoid a lesion of the vessels. But even in experienced hands 3 complications occurred. It is important to note, that this technique is not simple and involves the risk of complications. The surgeons need to be trained in surgery of the upper abdomen. The current literature (Tab. III) encompasses relatively few papers on celiac artery compression in children and adolescents compared to adults. The reported results vary broadly,

from 36 – 100 % symptom free at follow up. Younger patients seem to have a better outcome than adults. This might be a consequence of the aforementioned secondary stenosis of the vessel. External compression of the celiac artery can result in hyperplasia of the intimal layer and fibrosis of the vessel wall. An intrinsic or secondary stenosis can develop. In this situation we speak about fixed, respiratory-independent stenosis. In the case of secondary fixed stenosis balloon angioplasty or stenting can be discussed after external decompression of the artery [10]. Persistent stenosis of the celiac artery is only symptomatic, if the superior mesenteric artery is also stenotic, or if there are vascular gastric abnormalities present. Endoluminal therapy of celiac artery stenosis is associated with a high degree of recurrent stenosis [32]. Therefore, this method is not suitable for primary treatment of CACS, since external compression as the underlying cause remains unaffected. In the case of recurrence, complete initial diagnostic procedures have to be repeated. That should be the prerequisite for assessment of indication to redo-surgery. We observed 4 patients developing a recurrence after an initial symptom free interval of 6 – 12 months. In two patients we did a minimally invasive redo operation with conversion to an open operation in one. In another case we opted for a primarily open operation since in the first operation a conversion had already become necessary. All three patients became symptom free again. Redo decompression was always hampered by adhesions. It is basically more ambitious for the surgeon to free the celiac artery again. In another patient we did a simultaneous laparoscopic celiac artery decompression and a Nissen fundoplication for gastroesophageal reflux. Gastroesophageal reflux is a well-

known complication in patients with low insertion of the diaphragm since both the aortic and the esophageal hiatus may be affected. If so, both operations should be done simultaneously. The additional effort is acceptable and a second operation would be more difficult due to the adhesions.

Conclusions The diagnostics of chronic abdominal pain in children and adolescents should include a color Doppler sonography to rule out a celiac artery compression syndrome. We see an indication for operation in patients with characteristic symptoms and a relevant decline of the quality of live, with detected typical findings at Doppler sonography and MR angiography. The assessment of indication for surgical treatment requires a comprehensive exclusion of all relevant differential diagnoses. Laparoscopic decompression of the celiac artery is reliable and a less invasive procedure with excellent results in children and adolescents. It is a safe technique in well-experienced hands.

Conflicts of interest There are no conflicts of interest existing.

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Correspondence address Dr. med. Annegret Klimas, MD Department of Pediatric Surgery and Pediatric Urology HELIOS Klinikum Erfurt Nordhäuserstrasse 74 99098 Erfurt Germany [email protected] Submitted: 09.12.2014 Accepted after revision: 18.01.2015