J Neurogastroenterol Motil 2023; 29(2): 200-207  https://doi.org/10.5056/jnm22158
A Median Arcuate Ligament Syndrome Could Be Re-termed as a Nutcracker Celiac Ganglion Abdominal Pain Syndrome
Ji Eun Kim,1 Mira Kang,2,3,4 Ok Soon Jeong,5 and Poong-Lyul Rhee1*
1Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea; 2Health Promotion Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea; 3Digital Innovation Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea; 4Department of Digital Health, SAIHST, Sungkyunkwan University School of Medicine, Seoul, Korea; and 5Department of Data Service, Samsung Medical Center, Seoul, Korea
Correspondence to: *Poong-Lyul Rhee, MD, PhD
Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea
Tel: +82-2-3410-3409, Fax: +82-2-3410-6983, E-mail: plrhee@gmail.com
Ji Eun Kim and Mira Kang contributed equally to this work.
Received: September 10, 2022; Revised: November 24, 2022; Accepted: December 1, 2022; Published online: January 31, 2023
© The Korean Society of Neurogastroenterology and Motility. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background/Aims
Median arcuate ligament syndrome (MALS) is known as chronic recurrent abdominal pain related to compression of the celiac artery by the median arcuate ligament. We aim to seek the specific mechanism of the pain by evaluating symptoms and radiological characteristics on abdominal CT scans.
Methods
We analyzed 35 patients who visited the emergency room for recurrent abdominal pain after cholecystectomy. We classified the characteristics of patients as 4 clinical components and 2 radiological components. We defined the sum of weighted clinical scores and weighted radiological scores as nutcracker ganglion abdominal pain syndrome (NCGAPS) scores. We categorized the patients into 3 groups classified by the degree of NCGAPS scores. The 3 patients with top-3 NCGAPS scores were recommended for CT angiography.
Results
When the suspicion was graded by NCGAPS scores, post stenotic dilatation was significantly different among all groups (P < 0.001). The clinical components of pain varied positional or respirational change and continuous pain were significantly different among all the groups (P < 0.01). NCGAPS scores can remarkably differentiate highly suspicious patients in comparison to simply combined scores. Only 1 patient in the highly suspicious group by NCGAPS scores took the CT angiography and was confirmed with NCGAPS.
Conclusions
We suggest renaming MALS as NCGAPS, nutcracker celiac ganglion abdominal pain syndrome, to better explain the mechanism of the recurrent abdominal pain. Further studies on the diagnostic cutoff of clinical and radiological scores of NCGAPS are needed not to miss the diagnosis of NCGAPS.
Keywords: Abdominal pain; Ganglia, sympathetic; Median arcuate ligament syndrome
Introduction

Median arcuate ligament syndrome (MALS) is known as chronic recurrent abdominal pain related to compression of the celiac artery by the median arcuate ligament.1-3 MALS is also called celiac axis syndrome or Dunbar syndrome, a case series that was reported by Dunbar in 1965, but the identity as a disease is not clear, and it is rarely reported.3-6 Two hypotheses of MALS etiology are well known, one due to the decrease in intravascular blood flow due to compression of the celiac artery as the pathogenesis, and the other due to overestimation by the celiac ganglion.7 Because the mechanism of MALS is unclear and it is not included in the diagnostic category for abdominal pain, some case reports of MALS have been described with rare congenital diseases or gastroparesis.8 It is not easy to diagnose MALS in patients with abdominal pain because the etiology is not clear and is not considered a substantial cause of abdominal pain.9

Functional gastrointestinal (GI) disorders are diagnosed and classified using the Rome criteria.10 Considerable efforts have been made to evaluate patients with abdominal pain and dyspepsia such as functional GI classification according to the Rome criteria. However, some patients do not fall under the classification. A large number of patients with abdominal pain undergo psychiatric evaluation and may even take psychiatric medications.11 Some patients visit the emergency room (ER) with severe abdominal pain enough to wake up from sleep. The pain can be varied by changes in position, independent of eating or defecation. Some patients come to the ER with recurrent severe pain even after cholecystectomy for asymptomatic gallbladder (GB) stones or cholecystitis, and they are still suffering by not knowing the cause of the pain.12-14

Several studies on MALS have been conducted, but the previous studies had focused on imaging tools and did not deal with the clinical implications in detail. There was a study that analyzed the compression of blood vessels into the radiological image to see if there was post-stenotic dilatation or not, but it was not clinically meaningful.15 There were studies by surgeons with different ideas on surgical correction,16,17 but it was questioned why many physicians do not consider MALS as a differential diagnosis in patients with chronic abdominal pain of unknown cause. We thought that the characteristics of the pain in these patients are important and the mechanism of the pain is eventually the compression of the celiac trunk ganglion by medical arcuate ligament based on our case series.18 Thus, we would like to suggest MALS as nutcracker celiac ganglion abdominal pain syndrome (NCGAPS) so that the patients and physicians can easily understand the cause of pain.

We would like to find the cause and mechanism of pain in patients suffering from abdominal pain without a definite etiology. Therefore, we are proposing a mechanism-based scoring system made out of clinical and radiological characteristics and suggesting a diagnostic process for NCGAPS.

Materials and Methods

Study Design, Setting, and Participants

This study is a single-center retrospective cohort study conducted at Samsung Medical Center, a tertiary academic institution in Seoul, South Korea. We screened 67 patients who visited the ER for abdominal pain after cholecystectomy without post-operative complications such as GB perforation or GB adhesion between 2016 and 2018. We excluded patients who did not undergo CT scan (n = 3), have cancers (n = 15), have CT without sagittal view images (n = 5), or CT showing irrelevance of MALS (n = 4). Patients under the age of 18 were excluded (n = 1).

Among the 39 eligible patients, we further excluded 2 patients with difficulties in evaluating post-dilatation or celiac indentation on CT scan and 2 patients who did not respond to the phone survey. Finally, a total of 35 patients were analyzed (Fig. 1). We reviewed the electronic medical records to obtain variables for each patient for inclusion, exclusion, and outcome assessment. The data underlying this article cannot be shared publicly given the privacy of the individuals who participated in the study. The data will be shared on reasonable request to the corresponding author. Data for additional information was extracted from the Clinical Data Warehouse Darwin-C of Samsung Medical Center for this study. The study protocol was reviewed and approved by the Institutional Review Board at Samsung Medical Center (IRB No. 2022-01-020-002). This study was conducted by the principles of the Declaration of Helsinki. Patient information collected in this study was used only for patients who consented to access the electronic medical records, and only patients who consented to the phone questionnaire were included.

Figure 1. Patients flow chart. ER, emergency room; GB, gallbladder; CBD, common bile duct; RCC, renal cell carcinoma.

Variables and Definition

We collected the following variables at the time of ER visit: age, sex, body mass index (BMI), the total number of ER visits, and characteristics of abdominal pain.

Clinical scores were given by the patient’s response to detailed characteristics of abdominal pain via phone survey. We gave a clinical score of 1 for each of the following symptoms: (1) pain with positional or respirational change, (2) continuous pain, (3) pain not associated with meals or defecation, and (4) repeated ER visits more than 2 times. Then, we used total clinical scores and classified the patients into 3 groups according to the degree of clinical suspicion as the following: (1) a score 1 as non-suspicious, (2) a score 2 or 3 as weakly suspicious, and (3) ≥ 4 as highly suspicious. In the radiological component, we gave a radiological score of 1 for each of the following: (1) post-stenotic dilatation and (2) celiac trunk indentation. Then, we used total radiological scores and classified the patients into 2 groups according to the degree of radiological suspicion as the following: (1) a score < 1 as weakly suspicious, (2) a score ≥ 1 as highly suspicious. When the celiac artery was compressed by median arcuate ligament, 2 pathognomic radiological signs by pressure had occurred. One is post-stenotic dilatation at distal part due to flow. And the other is the celiac trunk indentation sign. We drew and presented a simple schematic diagram based on actual CT scan and CT angiography (CTA) images of patients that had been previously published (Fig. 2 and Supplementary Fig. 1).

Figure 2. Lateral view of nutcracker celiac ganglion. NCGAPS, nutcracker ganglion abdominal pain syndrome.

We defined the sum of weighted clinical scores and weighted radiological scores as NCGAPS scores. Weighted clinical scores were defined by multiplying 4, 3, 2, and 1 in order of clinical components, and weighted radiological scores were defined by multiplying 4, and 2 in order of radiological components. We gave 4 weighted points for post stenotic dilatation, the most important factor in radiological characteristics. Then 2 points were weighted for celiac indentation sign. As for clinical components, 4 weighted points were given when the pain was relieved by inspiration or the change in degree of pain by position, for instance, pain aggravated while lying down and relieved when getting up. This means the pain varied by migration of the diaphragm. Continuous pain was weighted 3. The pain not associated meals or defecation was weighed 2. The recurrent pain was weighted 1 (Supplementary Table 1).

The NCGAPS score was classified into 3 groups according to the degree as the following: (1) a score of < 5 as non-suspicious, (2) a score of 6-13 as weakly suspicious, and (3) a score of ≥ 14 as highly suspicious group.

Patients in the highly suspicious group by NCGAPS scores were recommended to undergo CTA.

Statistical Methods

The values are expressed as the median (range) or mean (standard deviation) for continuous variables and the number (%) for categorical variables. To compare the difference between 3 groups, the categorical variables were applied to the chi-square test or Fisher’s exact test, and the continuous variables were tested using the one way ANOVA test or Kruskal-Wallis test. Bonferroni correction method or Dwass, Steel, Critchlow-Fligner method was performed to correct for multiple comparison. A P-value less than 0.05 was regarded as statistically significant. All statistical analyses were performed using SPSS Statistics version 27.0 (IBM Corp, New York, NY, USA).

Results

Characteristics of Patients Categorized by Clinical Scores

The baseline characteristics of the study patients are summarized in Table 1. Of a total of 35 patients, the mean age of suspicious patients was 50.0 years, and 16 patients (45.7%) were male. The mean BMI was 25.8 kg/m2.

Table 1 . Baseline Characteristics

A. Characteristics of Patients Categorized by Clinical Scores

VariablesTotal patients(n = 35)Non suspicious(n = 13)Weakly suspicious(n = 19)Highly suspicious(n = 3)P-value
Age (yr)50.0 ± 11.448.9 ± 11.048.8 ± 10.461.4 ± 17.50.199
Male16 (45.7)6 (46.2)9 (47.4)1 (33.3)> 0.999
BMI (kg/m2)25.8 ± 4.026 ± 6.025.6 ± 2.326.3 ± 2.00.938
Radiologic component
Post stenotic dilatation18 (51.4)4 (30.8)11 (57.9)3 (100)0.061
Celiac trunk indentation20 (57.1)6 (46.2)13 (68.4)1 (33.3)0.350

BMI, body mass index.

See Supplementary Table 1 for detailed scoring.

Category by clinical scores: non suspicious: 1, weakly suspicious: 2 or 3, highly suspicious: ≥ 4.

Data are presented as mean ± SD or n (%).

B. Characteristics of Patients Categorized by Radiological Scores

VariablesTotal patients (n = 35)Weakly suspicious (n = 13)Highly suspicious (n = 22)P-value
Age (yr)50.0 ± 11.447.0 ± 9.351.7 ± 12.40.245
Male16 (45.7)6 (46.2)10 (45.5)0.968
BMI (kg/m2)25.8 ± 4.024.7 ± 5.026.4 ± 3.10.218
Clinical components-
Positional or respirational change7 (20.0)2 (15.4)5 (22.7)0.689
Continuous5 (14.3)2 (15.4)3 (15.0)> 0.999
Not associated meals & defecation22 (62.9)6 (46.2)16 (72.7)0.157
Recurrent351322-

BMI, body mass index.

See Supplementary Table 1 for detailed scoring.

Category by radiological scores; weakly suspicious < 1, highly suspicious: ≥ 1.

Data are presented as mean ± SD or n (%).



We categorized the patients into 3 groups according to clinical scores. There was no difference in the gender distribution of each group (P > 0.999), and there was no statistical difference in BMI with an average of 26 ± 6.0, 25.6 ± 2.3, and 26.3 ± 2.0 in the non-suspicious, weakly, and highly suspicious groups, respectively (P = 0.938). When radiological evaluation variables were investigated in the clinically suspicious group, the number of patients with post stenotic dilatation was 18 (51.4%), and 20 patients (57.1%) had celiac trunk indentation. In the highly clinically suspicious group, all 3 patients (100.0%) showed post stenotic dilatation. In the weakly group, 11 out of 19 patients (57.9%) showed post stenotic dilatation (P = 0.061). The most common celiac trunk indentation sign was noticed in 1 patient (33.3%) in the highly clinically suspicious group and 13 patients (68.4%) in the weakly suspicious group, but it was statistically insignificant (P = 0.350) (Table 1A).

Characteristics of Patients Categorized by Radiological Scores

We categorized the patients into 2 groups according to radiological scores. The mean age in the weakly suspicious group was 47.0 ± 9.3, which was not statistically different from 51.7 ± 12.4 in the highly suspicious group (P = 0.245). In the highly radiologically suspicious group, the mean BMI was 26.4 ± 3.1. When clinical evaluation variables were investigated in the highly radiologically suspicious group, the number of patients with positional or respirational change was 5 (22.7%), continuous was 3 (15.0%), not associated meals, and defecations were 16 (72.7%), and 22 patients had recurrent episodes (Table 1B).

Characteristics of Patients Categorized by Nutcracker Celiac Ganglion Abdominal Pain Syndrome Scores

We categorized the patients into 3 groups according to NCGAPS scores. There was no difference in the gender distribution of each group (P = 0.691), and there was no statistical difference in BMI with an average of 25.7 ± 5.6, 25.8 ± 2.9, and 26.3 ± 2.0 in the non-suspicious, weakly, and highly suspicious groups, respectively (P = 0.972). The post stenotic dilatation was significantly different between non-suspicious group and weakly suspicious group, and between weakly suspicious and highly suspicious group (P < 0.001). The celiac trunk indentation was significantly different between non-suspicious group with weakly suspicious group (P = 0.011). Positional or respirational change were significantly different among all groups comparisons (P = 0.002). Continuous components were significantly different among all groups comparisons (P = 0.001). The clinical component of “not associated meals and defecation” was significantly different between non-suspicious and weakly suspicious group (P = 0.007). When suspicion was graded by NCGAPS scores, all the clinical components were well differentiated (Table 2). But when we categorized groups by simple combined scores, continuous component was not statistically different among all the groups (data not shown). Figure 3 shows the difference in simply combined scores and NCGAPS scores categorized by clinical scores. The median of scores was 1 (minimum [min] 1, maximum [max] 3) by combined score, and 1 (min 1, max 7) by NCGAPS score in the non-suspicious group. The median was 4 (min 2, max 5) by combined score and 9 (min 3, max 13) by NCGAPS score in the weakly suspicious group. In the highly suspicious group, the median was 5 (min 5, max 6) by combined score and 14 (min 14, max 16) by NCGAPS score. Both scores of simply combined scores and NCGAPS scores showed the significant difference according to categorized by clinical scores. But NCGAPS scores based on summation of weighted scores for clinical and radiological components can remarkably differentiate highly suspicious patients in comparison to simply combined scores (Fig. 3).

Table 2 . Characteristics of Patients Categorized by Nutcracker Ganglion Abdominal Pain Syndrome Scoresa

VariablesNon
(n = 13)
Weakly suspicious (n = 19)Highly suspicious (n = 3)P-value
Age (yr)49.5 ± 11.148.5 ± 10.361.4 ± 17.50.193
Male5 (38.5)10 (52.6)1 (33.3)0.691
BMI (kg/m2)25.7 ± 5.525.8 ± 2.926.3 ± 2.00.972
Radiologic component
Post stenotic dilatationb015 (79.0)3 (100)< 0.001a < b, a < c
Celiac trunk indentationb4 (30.8)15 (79.0)1 (33.3)0.011a < b
Clinical component
Positional or respirational changeb04 (21.1)3 (100)0.002a < c, b < c
Continuousb02 (11.1)3 (100)0.001a < c, b < c
Not associated meals and defecationb4 (30.8)15 (79.0)3 (100)0.007a < b
Recurrent13193-

aNutcracker ganglion abdominal pain syndrome scores = weighted clinical scores + weighted radiological scores.

bBonferroni or Fisher combination method was applied to correct for multiple comparison.

BMI, body mass index.

See supplementary Table 1 for detailed scoring.

Category by combined scores: a, non < 5; b, weakly suspicious: ≥ 6 and < 14; c, highly suspicious ≥ 14.


Figure 3. The nutcracker ganglion abdominal pain syndrome (NCGAPS) versus simply combined scores in 3 groups categorized by clinical scores. DSCF, Dwass, Steel, Critchlow-Fligner.

The 3 patients in the highly suspicious group by NCGAPS scores were asked to perform CTA. However, only 1 patient took the CTA and was confirmed with NCGAPS (Table 3). Supplementary Table 2 shows the detailed scoring components on individual subjects.

Table 3 . Clinical and Radiological Characteristics in Subjects With Top 3 Nutcracker Ganglion Abdominal Pain Syndrome Scores

Patients No.Weighted clinical scoresWeighted radiologic scoresNCGAPS scoresNote
Positional or respirational changeContinuousNot associated meals or defecationRecurrentPost stenotic dilatationCeliac trunk indentation
S143214216Confirmed by CTA
S243214014
S343214014

NCGAPS, nutcracker ganglion abdominal pain syndrome; CTA, computed tomography angiography.

See supplementary Table 1 for detailed scoring.

CTA scan was not performed in S2 and S3 for personal reasons.


Discussion

In this study we suggest a new clinical term, NCGAPS, instead of MALS and a novel diagnostic algorithm (Supplementary Fig. 2). Among 35 patients who had severe pain enough to visit the ER even after cholecystectomy without complications, 3 patients were classified as highly suspicious NCGAPS score groups, and 1 patient was confirmed with NCGAPS by CTA. As for the remaining 2 patients, NCGAPS could not be confirmed since they did not undergo CTA for personal reasons.

According to most studies that have been reported before, it has been done only through radiologic features from a variety of patients who have shown no symptoms to patients who have severe abdominal pain. We focused on the mechanism of development of the pain and by changing the term of the disease, and it may help physicians to more fully understand the disease and diagnose better. If the name is changed to make it easier to understand, many doctors and patients will be able to identify the origin of the disease, then achieve better diagnosis, and be also diagnosed. NCGAPS is overlooked as a cause of abdominal pain because it is still considered a very rare disease and the mechanism is unclear.19 Many physicians and radiologists focus on the operation site or the organs in the pain area. Without finding the organic disease, it is looked at as a functional disorder or a psychiatric disease. Due to inconsistent definitions of MALS, the appropriate treatment is a subject of debate.20 Also, as for rarely diagnosed MALS patients, some are treated with surgery to alleviate pain,21 however, the benefit of the surgical treatments is debated. In a previous study, 5 out of 37 patients had typical symptoms, such as postprandial abdominal pain, vomiting, and/or weight loss, and 32 were without typical symptoms. More than half of the patients had collateral circulation and other complications such as an aneurysm or obstruction.15 Another study suggested exclusion criteria for the diagnosis of MALS and treatment methods such as ganglionectomy and ligament release.2 These studies have not focused on the clinical diagnostic method of MALS in depth considering symptoms such as reversible pain by positional or respirational change. Moreover, they have dealt mostly with the imaging diagnostic approaches.22 If the mechanism of abdominal pain in MALS is decrease in blood flow due to celiac artery compression, there should be evidence of ischemic tissue damage, but we could not find any ischemic evidence in the liver or stomach in our patients according to liver function profiles, CT, or endoscopy. Therefore, the possibility of an ischemic mechanism due to vascular compression is extremely low.23

Recently, our research team published a case series of 4 confirmed NCGAPS patients. These 4 patients complained of pain for a long time, and one of them had a history of cholecystectomy due to severe abdominal pain but could not be diagnosed with NCGAPS for 20 years. Symptoms of all 4 patients were improved by meloxicam, gabapentin such as neurologic agents, and pain killers.18 In one case, the pain was dramatically decreased from Numeric Rating Scale (NRS) 10 to NRS 2 points after medication. This suggests the pathogenesis of NCGAPS is ganglion compression. If the patient does not respond to medication, then surgical revision of the median arcuate ligament with ganglionectomy should be considered. We have been treating MALS medically but not surgically for 2 reasons. First, if the pain disappears when the compression of the CG by the MAL is released naturally or through a series of motions, such as standing up or lifting the MAL through thoracic breathing, then we consider the patients as having recurrent abdominal pain with a reversible condition. However, if the compression continues irreversibly, then the pain becomes intolerable and surgical correction is needed for complete remission. Second, the strength of CG compression varies according to the tightness of the MAL. Depending on the compression intensity, the pain can lessen by pain modulators such as neuropathic pain or NSAIDS, if then medical treatment should be considered instead of surgical procedures. However, if the pain is medically irresponsive, surgical correction is the ultimate treatment for MALS for now. Although there are limitations, from the cases we have experienced, there was no patient who had an irreversible condition or was medically irresponsive, so surgery was not necessary.

In our study, 1 NCGAPS patient out of 35 candidates was confirmed by a CTA. In another words, NCGAPS is not as rare as expected. CTA is necessary for the confirmative diagnosis of NCGAPS. However, CTA is not performed in most patients with unexplainable recurrent abdominal pain because patients do not think of NCGAPS as the cause, but it should be considered. Some studies have suggested that change of pulse volume amplitude by doppler ultrasonography would be an appropriate tools for diagnosis with MALS.24 We look forward to performing more studies on diagnostic cut off of peak velocity or deflection-angles in the future.

Our study suggests a diagnostic process of abdominal pain of unknown etiology. First, exclude organic GI disease by abdomen and pelvis CT scan and esophagogastroduodenoscopy. After excluding the problem of organic GI disease, listen to patients’ symptoms in detail, such as pain alleviated with positional change/deep inspiration or pain not associated with meals and defecation. Review radiological landmarks including post-stenotic dilatation or celiac indentation on sagittal view images of the abdominal CT scan. Calculate NCGAPS scores which are the weighted summation of clinical and radiological scores. If NCGAPS is highly suspicious, CTA should be performed (Supplementary Fig. 1).

This study has some limitations as it is a retrospective study focusing on medical records. However, we reinforced the medical information as much as we can through a survey by phone questionnaire. We used weighted clinical and radiological scores for NCGAPS scores according to the degree of importance based on our experience, therefore, NCGAPS should be validated in the next prospective study in the future. Due to limited access to CTA, most patients in this study did not undergo CTA. Thus, we could not exclude NCGAPS in the patients who did not undergo CTA. In this study, 1 patient was confirmed with NCGAPS by CTA and it shows NCGAPS is not as rare as it seems.

In conclusion, we suggest renaming the name of MALS as NCGAPS, nutcracker celiac ganglion abdominal pain syndrome, to better explain the mechanism of the recurrent abdominal pain and to raise awareness of the cause of the pain. Only when the etiology of pain is emphasized and the term is easy for patients to understand, gastroenterologists will be alert not to miss the proper diagnosis. Further studies are needed on the diagnostic cutoff of clinical and radiological scores of NCGAPS.

Supplementary Materials

Note: To access the supplementary figures and tables mentioned in this article, visit the online version of Journal of Neurogastroenterology and Motility at http://www.jnmjournal.org/, and at https://doi.org/10.5056/jnm22158.

Financial support

None.

Conflicts of interest

None.

Author contributions

conceptualization, data curation, formal analysis, methodology, and writing of original draft: Ji Eun Kim and Mira Kang; data curation: Ok Soon Jeong; supervision: Poong-Lyul Rhee; and conceptualization, data curation, and methodology: all authors review and editing. All authors read and approved the final draft submitted.

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