Article, Gastroenterology

Cecal volvulus in long-distance runners: A proposed mechanism

Cecal volvulus in long-distance runners: A proposed mechanism

Participation in marathons and other endurance exercise, including formal sporting events such as triathlons, and the “Ironman” challenge are steadily increasing [1]. Specifically, the popularity of marathon run- ning has increased dramatically: from an estimated 25,000 marathon finishers in 1976, to N500,000 in 2015; this represents a 20-fold increase in the past 4 decades [2].

The benefits of regular physical activity are well-documented; how- ever, participation in endurance exercise is not without risk. Long- distance runners are susceptible to musculoskeletal injuries, electrolyte imbalances, cardiovascular events, dermatologic conditions, genitouri- nary syndromes and gastrointestinal (GI) side effects including ische- mic colitis [3-9].

Exercise-related GI side effects include nausea, abdominal pain, diar- rhea, and hematochezia; these are more frequent in runners as com- pared to participants in other endurance sports, such as cycling and swimming. These GI side effects are likely related to mechanical forces on the body, forces that are 2 times greater in running than in other en- durance sports [10].

The general understanding has been that redundant or hyper- mobilized segments of the colon and colonic mesentery predispose to colonic volvulus [11]. Twisting of the large bowel occurs in the seg- ments of the colon where the mesentery is thin and narrow. Inadequate cecal fixation to the retroperitoneum is thought to predispose to cecal volvulus (CV), which is a twisting of the cecum, Ascending colon, and terminal ileum around the ileocolic mesentery. In up to 22% of human cadavers studied, the ascending colon was adequately mobile to allow for a CV [12]. This ascending colonic laxity has been characterized as “mobile cecum syndrome”; it was previously ascribed to a lack of fusion of the right colonic mesentery to the lateral abdominal wall and retroperitoneum [13]. Other proposed causes include a history of prior surgery, colonoscopy, multiple pregnancies, and colonic obstruction [13]. We propose another cause of CV: long-distance running and walking.

We report 6 new cases and 2 previously reported cases [14] of CV in endurance athletes. All patients underwent emergent Right hemicolectomy and primary ileocolic anastomosis. Our total of 8 cases add to the evidence supporting the association between CV and long- distance running and walking. We believe that repetitive mechanical stress to the cecum and right colon during running or fast walking leads to stretching and effacement of the colonic mesentery, predispos- ing to exercise-related CV.

We retrospectively reviewed the records of 6 patients with CV dur- ing our 9-year study period from 2009 through 2017. Each patient had a history of endurance running or walking. We describe a Mathematical model that may explain the correlation between running and cecal vol- vulus through biomechanical forces.

Patient 1 and Patient 2 were originally described in 1985 by one coauthor. We describe 6 additional patients with similar clinical characteristics (Table 1). The age range of the patients (4 women, 4 men) was 27 to 73 years. The mean body mass index (BMI) was

22.2. All patients were previously healthy had a history of frequent endurance exercise. One patient was pregnant when she developed

CV. Two patients were originally misdiagnosed in the emergency de- partment due to lack of concerning imaging findings and their other- wise good health. For 4 of the patients, preoperative imaging findings were consistent with CV (Fig. 1). Intraoperatively, all pa- tients were noted to have thin, lax, cecal and ascending colonic mes- entery (Fig. 2A). We propose that CV in our group of patients was associated with repetitive forces on the colonic mesentery associ- ated with long-distance running and walking.

Exercise offers Health benefits to nearly every organ system [3, 10]. Proposed GI health benefits include protection against the following: constipation, Diverticular disease, inflammatory bowel disease, choleli- thiasis, and colon cancer [10]. Yet exercise is also associated with ad- verse effects, including exercise-related transient abdominal pain (ETAP or “stitch”), gastroesophageal reflux, esophageal dysmotility, gas- tritis, abdominal cramping, nausea, vomiting, GI bleeding, iron defi- ciency “sports anemia”, diarrhea and more severe complications such as ischemic colitis [3-5].

The underlying mechanisms are not entirely clear, but vascular, hormonal, and mechanical factors have all been proposed etiologies of exercise induced abdominal pain [15]. Ischemia is thought to be the result of exercise-induced shunting of blood flow to the skeletal muscle, heart, lungs, and brain–leading to an 80% decrease in splanchnic blood flow [15]. Up to 85% of ultramarathoners test posi- tive for occult GI blood [16]. A variety of mechanical factors resulting from long-distance running and walking have also been proposed, including psoas muscle hypertrophy, the “cecal slap syndrome” (de- fined as the bruising of the cecum seen in marathon runners due to the repetitive ‘slapping’ of the posterior cecal wall against the ab- dominal musculature), and increased friction between the viscera and abdominal wall [17-19]. The mechanical stress during running may be due to repetitive up-and-down movements causing mechan- ical microtrauma to the abdominal viscera [10, 19, 20]. In animals, Strenuous exercise is a reported risk factor for the development of colonic volvulus [21]. In 1985, CV associated with thin mesentery and lax retroperitoneal attachments in 2 long-distance runners was reported by one of our coauthors [14].

The incidence of CV is reported to range from 2.8 to 7.1 per mil- lion people per year [22]. In the United States, CV accounts for up to 7% of colonic obstructions; it involves twisting of the bowel around its mesenteric base (Fig. 2B). The sigmoid colon is the most common site, followed by the cecum, which accounts for up to 40% of all cases of colonic volvulus [13, 23]. Sigmoid volvulus is more common in elderly men, while CV tends to occur in younger women [24]. CV often presents with nausea, vomiting, pain, and ab- dominal distention.

abdominal radiography detects CV in only about 50% of patients and is not diagnostically sensitive; nonspecific findings can include a dilated cecum with air-fluid levels and proximal small bowel distention. Com- puted tomography (CT) provides increased diagnostic sensitivity and findings include, a decompressed sigmoid colon with a dilated air- filled cecum, and the appearance of a closed loop obstruction; specific CT findings include the “X-marks-the-spot,” whirl, split-wall, and ileocecal twist signs [13, 23, 25]. Despite the increased sensitivity of CT scans, in many occasions, CV is only diagnosed at the time of surgery [26], therefore emergency care providers should be extra vigilant to avoid missing this diagnosis as occurred in our patient series.

Table 1

Characteristics of our patients. All eight presented with cecal volvulus. Wk = week.

Patient #

1

2

3

4

5

6

7

8

Age/Sex

42 M

60 M

39 M

73F

33F

37F

39F

29 M

BMI

19.5

19.9

22.8

20.8

26

23

22.1

23.7

Exercise

10 miles/wk; Ran N10

60 miles/wk; Ran 138

Runs N60

Ran N35

Walks N600

Runs 35 miles/wk; 3

Runs 40 miles/wk; 2

Daily elliptical use; 1

Habits

marathons

marathons

miles/wk

marathons

miles/yr

marathons

marathons

marathon

A

B

Fig. 1. Computed tomography (CT) scan (Patient 4; A- axial view, B- coronal view) on presentation to the emergency department. The cecum (depicted by white arrow) was notably dilated to 8.6 cm, with some evidence of air distal to the volvulus, suggesting a partial volvulus.

CV requires emergent surgical exploration and possible bowel resec- tion. Colonic perforation occurs in 25% of patients; gangrene, in 50%. Those 2 findings increase patient mortality by 3-fold [13, 23]. Currently, the procedure of choice is a right hemicolectomy with a primary

ileocolonic anastomosis [23]. surgical reduction and cecopexy has also been reported, as has endoscopic reduction, but these alternative proce- dures are generally not recommended due to their association with a high risk of recurrence [13, 23]. A recent study at our multi-

Fig. 2. A. Delivery of cecal volvulus through a laparoscopic hand-assist surgical incision prior to performing a right hemicolectomy. B. Intraoperative photographs of open surgery demonstrating the mobile cecal syndrome C. Illustrations demonstrating the sequence of events leading to cecal volvulus.

Fig. 3. A. Diagram representing the forces on the colon hanging from a mesentery, while the body is at rest. B. The opposing effect of adipose tissue on the mesenteric force (Ka = stiffness coefficient of adipose tissue, Km = stiffness coefficient of the mesentery, mc = mass of the colon). D. Mathematical equation describing colonic forces during exercise. (?Fm = load on mesentery, km = mesenteric elasticity constant, g = force of gravity, mc = mass of the colon, ?ymax = maximum colonic vertical displacement, ?s = change in position of the colon).

institutional, health care system found a total of 53 cases that presented over a 6 year period, i.e., approximately, 10 patients per year [27], how- ever, an exercise history is not routinely obtained from these patients. The six patients that we report in this study, were sequential patients that presented to a single surgeon who collected histories of endurance training.

We propose that exercise-related CV is the result of gradual stretching of the ascending colonic mesentery caused by repetitive vertical displacement (Fig. 3A, B, C). Our proposed mathematical model is based on physics of a spring [28]; during aggressive walk- ing or running, intraabdominal forces vertically displace the colon, altering the length and shape of the mesentery [29]. We propose that the cecal mobilization is proportional to the frequency of the forces resulting from vertical displacement, and that cecal hypermobilization is inversely proportional to the patient’s BMI and stride length. When these forces exceed the elastic recoil limit, mesenteric laxity results, and a propensity for CV develops.

Our equation describes the forces acting upon the colonic mesentery during exercise. It demonstrates that higher the vertical displacement (?ymax) of the body’s center of gravity, or the heavier the volume of stool (mc), the higher the increased load (?Fm) in the mesentery will be during walking or running. Therefore, if the body’s center of gravity is displaced more during running or fast walking than during normal walking, the mesentery will be subjected to higher loads. The magni- tude of the mesenteric load, the velocity, and the kinetic and potential energies all depend on the position of the colon as it falls from its max- imum vertical displacement to its maximum downward displacement during running.

We propose that cyclic mechanical forces of sufficient magnitude cause permanent elongation in biologic tissue [30, 31]. Our mathe- matical model may thereby explain why these forces lead to mesen- teric laxity, resulting in chronic stretching and thereby increasing the prevalence of GI symptoms in runners. Anatomic differences in

mesenteric laxity may also explain why some runners have a greater risk for CV. For example, visceral adipose tissue may ‘cushion’ the mesentery and protect against deformation (Fig. 3B). Visceral adi- posity may therefore prevent and diminish the mesenteric elonga- tion required for exercise associated CV according to our proposed mechanism; we note, none of our patients were obese, with an aver- age BMI of 22.2.

Exercise-related volvuli may be more prone to occur in the cecum rather than the sigmoid colon, as the cecum is larger in di- mension and can hold more liquid stool mass, thus making it heavier and, according to our equation, more prone to develop mesenteric laxity and volvulus. Small frequent stresses may not cause the mesentery to elongate, however, cumulative stresses over time may predispose to permanent mesenteric deformation and CV. As a living tissue and organ, the mesentery is expected to undergo remodeling as it is subjected to repeated loads. Mesen- teric remodeling may therefore alter the stiffness (km), on the yield point, the load over which permanent deformation occurs, and on the ultimate strength, the load at which tissue will tear [32]. To our knowledge, in addition to the two cases reported ear- lier [14], no other study has evaluated the proposed association between long distance running and CV. We acknowledge the lim- itations of our study; the retrospective nature of this study, rarity of presentation and limited sampling of cases precludes our abil- ity to determine causality. Additionally, 75% of the cases reported here, presented to a single provider who collected histories of long distance running, thus contributing to some selection bias. Clinical factors such as histories of chronic constipation, con- sumption of high-fiber diets, and late pregnancy, which have all previously been described as factors important in the develop- ment of CV may have confounded our results [24, 33, 34]. Our mathematical model attempts to explain the pathophysiological basis of CV development in athletes and may not directly explain

other associated GI symptoms such as nausea, vomiting, abdom- inal pain and dysmotility. These symptoms may have a multifac- torial, physiology origin and may be explained by the aforementioned vascular, mechanical and neurohormonal mech- anisms. More studies using animal models and prospectively col- lected clinical data on exercise habits are essential to further validate our hypotheses.

5. Conclusion

Given the increasing number of long-distance runners and walkers, exercise-related CV should be a part of the differential diag- nosis in those with abdominal pain. Our case series demonstrates a potential association between CV and long-distance running and walking in otherwise healthy patients. We propose that the repeti- tive vertical displacement of the colon during long-distance running and walking may be an independent risk factor for exercise-related CV, and emergency care providers need to be cognizant of eliciting a history of extreme endurance activities in patients presenting with clinical symptoms of colonic obstruction. Given the heteroge- neity in clinical presentation, and the non-specificity of imaging studies, providers may fail to attain an accurate diagnosis, and in these circumstances discerning exercise habits may be particularly valuable.

We acknowledge the generous support from the William Harmon Surgical Education Fund. We also acknowledge Harmon Design Studios Inc. for graphics and images; the late Dr. William G. Gamble, who was the first surgeon to suggest a link between cecal volvulus and long- distance running.

The authors have no relevant financial disclosures to report.

Brent D. Bauman Jennifer E. Witt Victor Vakayil* Shumaila Anwer Eric D. Irwin Mary R. Kwaan Timothy L. Pruett James V. Harmon

Department of Surgery, University of Minnesota, MMC 450, 420 Delaware St SE, Minneapolis, MN 55455, United States of America

*Corresponding author.

E-mail addresses: [email protected] (B. Bauman),

[email protected] (J.E. Witt), [email protected] (V. Vakayil), [email protected] (S. Anwerl), [email protected] (M.R. Kwaan), [email protected] (T.L. Pruett), [email protected] (J.V. Harmon).

https://doi.org/10.1016/j.ajem.2018.07.045

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