Abstract
Background/Aim: Primary omental torsion is uncommon, mimicking appendicitis and other acute abdominal pathologies. It often escapes diagnosis on imaging investigation or conventional open laparotomy. This study aimed to evaluate the effect of laparoscopy on the various parameters of this entity, including incidence, diagnosis, and treatment. Materials and Methods: A systematic review was performed, including PubMed and Scopus databases, without a time limit, following the PRISMA principles. A total of 16 articles from January 2000 to December 2023, corresponding to 56 children with primary omental torsion, complied with the research criteria. Results: Primary omental torsion was associated with obesity. Symptoms were right abdomen oriented, often compared to those of acute appendicitis. Preoperative ultrasound displayed low diagnostic accuracy, whereas computerized tomography diagnosed only two thirds of cases. In all patients, the vermiform appendix was normal. Conclusion: Laparoscopy affected both diagnosis and treatment of primary omental torsion in children. Easy peritoneal cavity access rendered possible the diagnosis of cases previously discharged as abdominal pain of unknown etiology. Combined with the increased pediatric obesity, it also affected primary omental torsion incidence. The recent pathogenetic theories may be better supported today, as laparoscopy provides a detailed view in situ, and facilitates harvesting of fat tissue from the omentum for molecular investigation. The diagnostic efficiency of laparoscopy is superior to ultrasonography and computerized tomography. Finally, the removal of the ischemic omentum is technically easier compared to the open laparotomy alternative with all the technical difficulties of traction of a vulnerable hemorrhagic tissue through a small incision.
Omental pathology is uncommon, with a reported incidence of 1:600 appendectomies during a period of 20 years in Australia (1), and 1:800 appendectomies in 30 years in the United States (2). Bush was the first to describe the idiopathic omental infarction in 1896 (3). Three years later, Eitel described the primary omental torsion (POT) as a cause of abdominal pain (4). Since then, approximately 400 patients with POT have been reported worldwide, with an age peak of 40-50 years, and with two thirds being males (5-7). POT incidence in the pediatric population is 0.1-0.5%, extracted mostly through surgical intervention for acute abdominal pain, attributed to possible appendicitis (8-12).
The omentum is the main defensive organ of the abdominal cavity, adopting an adhesive behavior to seal an impaired area (13). Increase of the omental blood flow and expansion of the omental stromal tissue occur as a response to stimulation (14, 15). Cells which express stem cell markers, inflammatory, and chemotactic factors, are produced (16-18). The activated stromal cells engraft onto the irritated sites and lead to the recruitment of inflammatory cells within the peritoneal cavity. The result is the formation of adhesive bridges (14, 19, 20).
The omentum may rotate along the axis of the distal right epiploic artery (2), either in a clockwise or counterclockwise direction (21, 22). Congenital developmental abnormalities and variations (bifid omentum, tongue-like projections, redundant omental veins, local fat accumulation) may facilitate torsion (23-27). The right part of the omentum, which is larger, heavier, and with independent mobility, is affected more frequently (22, 28). The aggressive omental behavior in association with anatomical and physiological factors (acute alteration of posture, digestion of excessive food, visceral fat associated inflammation) favor torsion, infarction, and finally necrosis.
POT symptoms are nonspecific. They mainly mimic appendicitis while older children and adults may also present with symptoms indicative of cholecystitis, perforation or peptic ulcer, and ovarian torsion (29, 30). During the early phases of torsion, traction of the omental root occurs, causing initially periumbilical pain, or pain at the xiphoid process (30). As congestion, ischemia and necrosis of the rotated segment develop, the pain adopts the characteristics of appendicitis, in many instances without the typical symptoms of appendiceal bacterial infection, such as nausea, vomiting, fever, tension, emergency, or diarrhea (31). Furthermore, the progress of the symptoms is slower compared to appendicitis (31). The clinical differential diagnosis in children may also include Meckel’s diverticulitis, mesenteric lymphadenitis, gastroduodenitis, or Crohn’s disease (22).
Diagnosis of POT may be performed using ultrasonography (US) and computerized tomography (CT) (32-35). Magnetic resonance imaging (MRI) has been used sporadically as well (36). Omental infarction imaging was first described by Puylaert (37). US nonspecific results may include free fluid in the pelvis or the right iliac fossa, or a hyperechoic mesentery (38, 39). The sonographic criterion for the diagnosis of omental infarct is the identification of an oval hyperechoic mass, adherent to the abdominal wall with a hypoechoic rim, located mainly at the right side of the abdomen, with the presence of a normal appendix (40, 41). In the CT, the density of the omental mass is not different from that of the abdominal wall fat (30). The location of a fatty soft tissue structure between the colon and the rectus abdominis sheath has been considered specific for the diagnosis with CT (30, 40). The infracted omentum is delineated as a fatty mass immediately deep to the parietal peritoneum, with secondary thickening and inflammation of the overlying anterior abdominal wall (24, 37, 42, 43). The presence of a vascular pedicle, and the whirl of the omentum are characteristic signs (30). A variety of diseases are included in the imaging differential diagnoses of omental torsion, such as mesenteric panniculitis, lipoma, liposarcoma, teratoma, angiomyolipoma, epiploic appendagitis, gossypiboma and tumours containing fat (44). Operative management is the gold standard treatment method. With the advent of laparoscopy, both diagnosis and treatment of POT have been affected. The first two reports of POT laparoscopic treatment in adults were published by Chung et al., and Gassner et al., (45, 46) while Gul et al., reported the first pediatric laparoscopic excision of necrotic omentum after POT, in a case series which included a 14-years-old boy (26).
In this systematic review, we aimed to investigate the impact of laparoscopy on the diagnosis and treatment of POT in children and discussed issues such as pathogenesis and clinical presentation of this uncommon entity. We also aimed to compare the diagnostic efficiency of laparoscopy with that of US and CT, and its therapeutic efficiency compared to conservative treatment and open laparotomy in this easy to treat morbidity, however until recently often escaping diagnosis.
Materials and Methods
We performed a systematic literature review with the following criteria for article types: original articles, case studies, case series, articles obtained in full text, articles in English, and articles in humans. No time limit was set for articles related to their research or publication. The databases used were PubMed and Scopus. The keyword combinations included [omental torsion], [omental infarct], [primary omental torsion], [children], [pediatric], [laparoscopic surgery], [laparoscopy].
The principles of the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) methodology were used for the analysis of the retrieved information (47, 48). A total of 16 articles published during a period of 23 years (January 2001-December 2023) were considered suitable for inclusion in the study (Figure 1, Table I). The chi-square test was employed to determine the correlation between qualitative independent variables. The statistical analysis was performed with the SPSS Statistical Software Package version 25 (IBM Corp., Armonk, NY, USA). The threshold for statistical significance was defined as p<0.05.
Flow diagram of literature search and article selection process according to the PRISMA guidelines.
Summary of the main findings of the articles included in the study.
Results
The study population included 56 children with a predominance of boys (n=44, 78.5%) (Table I). The sex of two patients was not reported in one study (49). The age range of the patients was 4-16 years. All articles were case reports or case series. The largest series from a single center included 17 patients (30).
The main clinical symptom which was present in every child with POT was abdominal pain. The initial distribution of pain involved the right lower (n=33 patients, 58.9%), right middle (n=8, 14.3%), right upper (n=7, 12.5%), left lower abdomen (n=2, 3.5%), the epigastrium (n=3, 5.3%), and the periumbilical (n=3, 5.3%) region. Few patients had gastrointestinal symptoms, such as nausea (n=9, 16.0%), vomiting (n=13, 23.2%), and clinical signs, such as rebound tenderness (n=6, 10.7%), and abdominal muscle guarding (n=21, 37.5%). It is of note that there were studies which mentioned the presence of a good appetite regardless of the presence of pain (9, 50). Low grade fever was reported in 15 (26.7%) patients. White blood cell count was moderately elevated in 20 (35.7%) patients, while c-reactive protein (CRP) was elevated in 21 (37.5%). A total of 46 (82.1%) patients were characterized as overweight or obese.
The outcomes of preoperative radiological investigation are shown in Table II. Preoperative US was performed in 44 (78.5%) patients. However, its diagnostic accuracy was low, as an inflammatory mass was diagnosed in only 5/44 (11.3%) patients. The most commonly reported outcome was the presence of free fluid in the peritoneal cavity (n=8, 18.1%). CT examination was conducted in 33 (58.9%) patients with a positive diagnosis in 24/33 (72.7%). MRI was recruited once, with a positive diagnostic outcome (36) (Table II).
Ultrasonography and computed tomography (CT) examination outcomes compared.
All patients of the study were submitted to laparoscopy. The main finding was a mass corresponding to the rotated, infarcted and gangrenous omentum. It was either pending free in the peritoneal cavity or adhered to various structures in the abdomen, i.e., the anterior or right abdominal wall, the lower abdomen or higher at the hypochondrium, near the hepatic margin, behind the liver, or at a right lumbar location. It was also adhered to the ascending colon, the cecum, even the sigmoid colon (21). Anatomic redundancy of the rotated right omental portion was mentioned (51). A total of 720° was the most severe twist described (22). The presence of free serosanguineous fluid in the abdominal cavity was characteristic (52). The vermiform appendix was found without inflammation in all 56 children. Except for one study (30) which reported a mean postoperative hospital stay of five days, the patients were discharged from the first to the third postoperative day. No significant postoperative complications were reported. One patient presented relapse of torsion after eight months (30).
Discussion
Though the outcomes of this systematic review were obtained from a limited study population, interesting insights on POT were obtained. It became obvious that laparoscopy created new perspectives which affected epidemiology, pathogenesis, diagnosis, and treatment.
How laparoscopy affected POT incidence. POT incidence has increased during the last twenty years. While older studies on large numbers of children reported an incidence of one case of omental infarction in 800 operations (2) for possible appendicitis, in more recent series the incidence was one in 275 operations (11). Moreover, Valioulis et al., reported two patients with primary omental torsion among 54 exploratory laparoscopies for acute abdominal pain (28), while Jukic et al., reported four cases among 244 children who underwent negative appendectomy (53). PubMed database search using the key words “primary omental torsion” and “children”, during the period 1950-2000 yielded 38 articles found on POT (rate 0.7 per year), while between 2001 and 2023, actually a half-time period, the rate of studies was doubled, (33 articles, rate 1.4 per year).
Increased childhood obesity is associated with increased POT incidence (7, 11, 39, 40). Furthermore, during the same period, the advent of laparoscopy rendered POT diagnosis more effective, favoring the balance between diagnosed and undiagnosed cases towards the first. Open laparotomy presents limited exposure of the peritoneal cavity (9), often accessing the ischemic omentum accidentally, during an excision of a normal appendix. This may result in the loss of undiagnosed cases of omental pathology. Presumably, as pediatric surgeons become more familiar with the use of the fine laparoscopic means, and as more pediatric centers adopt minimal invasive techniques, more cases previously labeled as abdominal pain of unknown origin on hospital discharge will be diagnosed properly.
Association of laparoscopy with insights on POT pathogenesis. Congenitally anomalous fragile blood supply to the right lower portion of the greater omentum renders this region easier to infarct (53). Venous engorgement after heavy meals or venous elongation produced by excessive weight of the greater omentum have been proposed as risk factors, since there is a higher prevalence of the syndrome in the obese population (54). Excessive gravitational traction is exerted by a larger omentum as well (24, 55). In these patients, the increased fat deposition may also outstrip the blood supply to the developing omentum. It has been proposed that not only the total amount of omental fat but the irregular distribution in obesity leads to the development of torsion (50). Children older than three years present increased fat deposition in the developing omentum in association with growth, which may be considered as a major predisposing factor (11). Furthermore, the greater accumulation of omental fat in males compared to females, may be associated with POT preponderance in obese boys (56). By the advent of laparoscopy, the theories described herein are easier to examine, as the panoramic view of the peritoneal cavity renders the diseased omentum visible in situ.
It is of note that the findings of this systematic review are in accordance with the relevant literature, as the younger patients were four-year-old, and most of them belonged to the spectrum of obesity. Moreover, POT was four times more common in the boys of the study, compared to girls. A total of 82.1% of children were found obese, verifying the association of obesity and torsion probability. It is obvious that laparoscopy offers, in particular in obese patients, a more convenient and less traumatic access to the diagnosis and treatment of POT, compared to a constricted access through a small incision in a thick abdominal wall.
Sudden alteration of the abdominal position and immediate increase of the abdominal pressure may induce rotation of the omentum (11). Mainly in children with the characteristics described previously, overeating, intestinal hyperperistalsis, overextension, sudden changes of body position, excessive exercise, and trauma may trigger omental torsion (25, 27, 57). We infer that such small torsions along the longitudinal axis may be asymptomatic, or with mild symptoms, such as recurrent moderate abdominal pain, affecting omental physiological reaction. Thus, in some cases a congestion and blood supply impairment, even small, may trigger the omental biological cataract of inflammation and adhesion. These conditions with a milder clinical presentation, may be definitively diagnosed with laparoscopy today.
We know that visceral fat is associated with the production of inflammatory response (58). The homeostasis of the visceral adipose regulatory T cell population, in the human omental fat, is a field of contemporary research. These cells play a critical role in controlling visceral fat inflammation by alleviating metabolic disease (58). However, this cell population is disrupted by obesity, which exacerbates inflammation and metabolic abnormalities. Studies support that these cells are even lost in obesity (59). Maybe the answer to our question on POT pathophysiology lies in these fatty omental cells. We suggest tissue sample acquisition in situ during laparoscopic surgery, for molecular investigation, in collaboration with molecular biologists specialized in obesity.
Verification of clinical presentation outcomes by laparoscopy. The POT symptoms depend on the degree and duration of torsion (30). The pain is usually sudden at onset with progressive exacerbation (7, 39, 50, 60). In approximately 90% of patients, the pain is located at the right side of the abdomen (27, 28). In the series of this review, most children (n=48, 85%) presented with a right abdominal distribution of symptoms.
Nausea and vomiting are encountered in 50% of patients with POT (55). In the series of our review, nausea was reported in one out of ten patients, while one out of four patients presented with vomiting. POT has also been presented as a hip pain and limp (61). Patients with POT may not seem as ill as those with acute appendicitis. Children with omental infarction are constitutionally well, hungry, afebrile and without elevated white blood cell count. This accounts for the delay in seeking surgical evaluation (24). Finally, in this study the right abdominal preponderance of symptoms is verified, as well as the fact that patients have a good appetite (9, 50).
The superiority of laparoscopy against US and CT as a diagnostic tool in POT. We must correlate the variability of the results with ultrasonography with two factors, both regarding the operator. The first is personal experience, ability and subjectivity. The ultrasound imaging findings are subtle and operator dependent (49). Second, we must not forget the operator’s subjective tendency in diagnosing acute appendicitis. No operator starts a pediatric abdominal ultrasound having in mind that certain patients might present an omental torsion, but the first asset of differential diagnosis is acute appendicitis. The overall diagnostic rate of omental torsion has been estimated at approximately 10% (62, 63). CT has proven to be the most accurate radiological diagnostic tool so far (30). Recently, Chen et al., reported a diagnostic accuracy of 70.59% in the largest series of POT cases in children reported in a single center (30).
US was accurate in 11.3% and CT in 72.7% in the study population of this review, where POT was confirmed with laparoscopy in 100% (Table II). In a statistical analysis performed in the study population of our review, CT proved to be a more reliable diagnostic tool compared to US (χ2=30.24441, p<0.001). Nevertheless, it missed one third of cases, which is a fair proportion. The diagnostic deficiency of both radiological methods renders laparoscopy a valuable tool not only from the aspect of therapy but also from that of diagnosis.
Practical operative benefits of laparoscopy. Conservative treatment with observation and supportive measures is an alternative option of management (32, 49). It has been advocated when diagnosis is made with CT (49, 64). Patients who benefit from this approach usually have localized moderate abdominal pain. It includes overnight observation, serial abdominal examinations, and continuous adjustment of the administered pain medications (49). In the absence of peritoneal signs, children with POT have been reported to be treated conservatively with complete resolution of abdominal pain. We must not forget that this is the point which in the past created cases of undiagnosed abdominal pain who had a favorable conservative outcome in the absence of radiological diagnosis. This deficiency ends with the advent of laparoscopy.
Laparoscopy can be effectively and safely performed in children (50, 65). The twisted omentum may be easily and safely excised laparoscopically. There were no major intraoperative or postoperative complications encountered in the research articles included in this review, and a rapid recovery with good cosmetic results was universally observed (50). Only one patient of the 56 of those included in our systematic review, with relapse of torsion after eight months, might be considered as the only long-term complication (30).
A great advantage of laparoscopic surgery is the adaptation of trocar placement for the achievement of the best and easier performance (51, 66). In conventional laparotomy all the work must be done through a small incision with restrictive optical ability that may lead to misdiagnosis and forces the surgeon to perform elaborate movements and manipulations either with instruments or with the fingers, especially in obese children. With laparoscopy, the trocars are placed after the localization of the lesion, with the most convenient result. Although removal of the intact lesion is the rule, segmental (piecemeal) removal has also been reported (45).
With laparoscopy, other common pathologies, such as the primary clinical target of acute appendicitis, secondary torsion, or infarction without torsion which presents similar radiological characteristics, were effectively diagnosed and treated (36, 40, 49). In the study population of this review, the treatment of the patients with the most serious clinical presentation who were initially treated conservatively, was switched to laparoscopic exploration (40, 49).
A final comment should be made on the postoperative course and hospital stay. Although patients who were submitted to laparoscopy were those who presented more serious clinical symptoms and signs, their postoperative stay in the hospital was short (67, 68). Most of the patients were discharged from the hospital from the first to the third postoperative day. Delayed surgical or conservative treatment may lead to complications, such as abdominal abscess, sepsis and adhesion formation (22, 68).
Study limitations. The main limitation of the study is the small population, as POT has been considered as a rare disease so far, and laparoscopy is actually a novel technique in children. However, we believe that in the next years, with the widespread performance of minimal invasive surgery, even robotic surgery in pediatric patients, the epidemiological indexes will be modified to more representative numbers. Finally, with the inclusion of articles only written in the English language, we may have excluded some interesting articles in other languages.
Conclusion
POT diagnosis in children has become easier with the advent of laparoscopy in pediatric surgery during the last twenty years. The identification of the twisted ischemic omentum is timely feasible, with minimal surgical tissue damage and early hospital discharge, together with a full inspection of the peritoneal cavity. The possibility of diagnosing different pathologies is more efficient as well. Although CT presents a certain accuracy, it may miss a fair number of POT cases. Management is also easier, with the safe removal of the gangrenous omental tissue without the difficulty, stretching, and elaborate manipulations of conventional open surgery, through a small incision, that is frequent in an obese child. Finally, pathogenesis theories may be postulated more definitively with immediate visualization of the entire peritoneal cavity. Furthermore, targeted acquisition of in situ material for histopathological and molecular investigation will shed more light on the pathogenesis of the primary omental reaction that leads to torsion.
Footnotes
Authors’ Contributions
VA and XS designed this study. Data collection and literature searches were performed by VA, XS, and AL. VA, XS, AL, CD, and DD performed the data analysis and interpretation. All researchers interpreted the data and contributed to the draft of the manuscript and figures. Finally, the article was revised and approved by all Authors.
Funding
There is no funding for the article.
Conflicts of Interest
The Authors declare that they have no conflicts of interest or financial ties in relation to this study.
- Received January 12, 2024.
- Revision received February 20, 2024.
- Accepted February 21, 2024.
- Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).