Prevalence, classification and characteristics of the coloileal reflux diagnosed by barium enema

Abstracts

OBJETIVO: Verificar, retrospectivamente, a prevalência do refluxo cecoileal diagnosticado pelo enema opaco, caracterizar sua distribuição etária e sexual e classificá-lo conforme o grau de intensidade. MATERIAIS E MÉTODOS: Foram revistos 715 enemas opacos, incluindo 268 homens e 447 mulheres com idade média de 54 anos. RESULTADOS: Dos 715 casos examinados, 46,5% apresentaram refluxo cecoileal, sendo 45% do tipo leve, 37,5% do tipo moderado e 17,5% do tipo severo. Refluxo cecoileal esteve presente em 48,3% das mulheres e em 43,6% dos homens. A distribuição percentual do refluxo cecoileal por faixa etária mostrou 46,1% nos indivíduos com menos de 21 anos, 42,1% nos indivíduos entre 21-40 anos, 49,8% nos indivíduos entre 41-60 anos e 44,7% nos indivíduos com mais de 60 anos. CONCLUSÃO: Refluxo cecoileal foi achado relativamente freqüente em nosso material, correspondendo os graus moderado e severo a 25% do material examinado. Aparentemente, não há associação entre seu surgimento e sexo ou idade. A etiopatogenia e conseqüências do refluxo cecoileal são ainda pouco conhecidas. Alguns estudos sugerem que o comprometimento de componentes da junção ileocecal, como os ligamentos, pode favorecer seu aparecimento. Entre as conseqüências prováveis, incluem-se a contaminação e alteração motora ileais, resultantes do material refluído do ceco.

Refluxo cecoileal; Válvula ileocecal; Junção ileocecal; Síndrome do supercrescimento bacteriano do delgado; Refluxo cecoileal no enema opaco

ORIGINAL ARTICLE

Prevalence, classification and characteristics of the coloileal reflux diagnosed by barium enema^*

Wellington Monteiro Machado^I; José Morceli^II

^IMedical Doctor Assistant at the Department of Medical Clinic, Botucatu Faculty of Medicine, Unesp

^IIMedical Doctor Assistant at the Department of Imaging Diagnosis, Botucatu Faculty of Medicine, Unesp

^{Mailing address}

ABSTRACT

OBJECTIVE: Retrospectively determining the coloileal reflux prevalence at the barium enema examination, characterizing its distribution by sex and age range and classifying it according to the intensity degree.

MATERIALS AND METHODS: 715 barium enemas were reviewed, being 268 of male patients and 447 of female patients, with average age of 54 years.

RESULTS: Of the 715 enemas performed, 46.5% showed coloileal reflux, classified as mild (45%), moderate (37.5%) and severe (17.5%). Coloileal reflux was present in 48.3% of female and in 43.6% of male patients. The coloileal reflux distribution by age range was 46.1% in individuals less than 21 years, 42.1% in individuals between 21–40, 49.8% in individuals between 41–60 and 44.7% in people more than 60 years old.

CONCLUSION: Coloileal reflux was a common finding, with 25% of them being classified as moderate or severe. Apparently, there is not a clear relationship between its occurrence and gender or age. The etiopathogenesis and consequences of the coloileal reflux remain still poorly known. Some studies suggest that the compromising of ileocecal junction components, like ligaments, could favor the coloileal reflux occurrence. Among the probable consequences, we could mention contamination and ileal motility disorders resulting from the material refluxed from cecum into the ileum.

Keywords: Coloileal reflux; Ileocecal valve; Ileocecal junction; Small bowel bacterial overgrowth syndrome; Coloileal reflux at the barium enema.

INTRODUCTION

Along the digestive tube, there are specialized muscular structures denominated sphincters with the main role of controlling the passage of the digestive tube contents from an organ into another⁽¹⁾. The compromising of this sophisticated function may bring a series of harmful consequences. Examples are innumerable: achalasia of the esophagus inferior sphincter (EIS) difficulting the movement of food through the esophagus or its hypotonia, favoring the gastric reflux and the appearance of the gastroesophageal reflux disease (GERD)^(2–5). Alteration of other sphincters % as the anal one % also are a common condition, determining the manifestation of fecal incontinence or intestinal constipation^(6,7). More scarcely, sphincters like the pyloric or Oddis also have been considered responsible for different clinic pictures^(8,9). But, there is another sphincter, whose roles and eventual disorders are still little known % that sphincter denominated ileocecal sphincter, also called ileocecal valve or, more comprehensively, ileocecal junction (ICJ)^(10–13). Located on the point at which the ileum joins the cecum, it separates two different ecological and functional environments and, apparently, has two highly relevant properties: it moderates the flow of intestinal contents from the ileum into the cecum and avoids the reflux of the plentiful cecal bacterial flora into the small intestine^(10,14–18).

There are many resources employed for studying and defining proximal and distal sphincters functions and disfunctions. However, for the intermediary sphincters, such resources are scarce. This disparity is partially justified by the ease for accessing the first ones and the difficulty for accessing the later ones. As a natural result, a huge progress has been achieved in the knowledge about anal and esophageal extremities sphincters, in terms of diagnoses, understanding of their function and a more adequate approach to the related pathological conditions. On the contrary, intermediary sphincters, like the ileocecal, in a difficult access site, have not benefited in the same proportion from the contemporary investigation methods available for extreme sphincters such as electric impedance, manometry, pHmetry, barostate. As a result, the knowledge about intermediary sphincters intrinsic characteristics and conditions resulting from its alterations is more limited and superficial.

As a consequence of the methodological limitations, the assessment of the CIJ has been scarcely reported^(16,19–22). In the few studies available, among the aspects that have attracted greater interest, are the sphincteric pressure measurement, both in rest and under stimulation, and evaluation of the sphincteric competence grade. In the distant past^(23–25), radiological studies brought into question the existence of an effective CIJ competence, so that the via rectal retrograde infusion of radiological contrast was proposed as an alternative way of studying the small intestine morphology, since the CIJ would not offer effective resistance to the free retrograde flow of the barium up to the small intestine⁽²³⁾. Nevertheless, to achieve such intent, high infusion pressures and special postural maneuvers were recommended, which certainly resulted in artificial situations likely to induce inadequate conclusions and consequences^(23–25). Diverging from these old concepts, recent studies have shown the considerable competence of the CIJ tolerating high levels of intracecal pressure, and offering a firm resistance to the occurrence of reflux into the small intestine^(26,27). Studies with animals and humans have shown that intracecal pressures can reach values above 80 mmHg without triggering a significant reflux into the ileum, reflecting the CIJ capacity of effectively resist to the increased colonic pressures⁽²⁶⁾.

Presently, the colon radiologic contrast-enhanced study is performed by means of barium enema. In this method, the rectal administration of contrast agent is made without using excessive pressure, but just in the necessary level to ease the barium migration up to the cecum, so that, most probably, such pressure is not sufficient to overcome the barrier corresponding to the CIJ, also considering that this barrier is constituted not only of the sphincteric pressure but also of anatomic angulations and coloileal ligaments which substantially reinforce its efficacy^{(19,21,26,27)}. Therefore, it is reasonable to presume that significant coloileal reflux is not likely to happen in a high number of barium enemas and that its occurrence probably happens due to the compromising of the anti-reflux barrier elements, similarly to that described for the gastroesophageal reflux. In this kind of reflux, there is also a barrier constituted of sphincter, angulations (Hiss angle) and ligaments (phrenoesophageal) which, when isolatedly or jointly compromised, allow the manifestation of the GERD^(4,5).

The utilization of the Radiology for identifying the GERD and its consequences is a recognized method^(28–30) with quite acceptable sensitivity and specificity, even if compared to more recent methods like esophagel pHmetry^(28,29). Nevertheless, the same application has not been assigned to the barium enema for coloileal reflux detection, since in several radiological centers this finding description in not even mentioned in a systematic, but fortuitous way. The reason for such a conduct possibly lies in the tradition and incomplete knowledge about the meaning of the coloileal reflux. Tradition, with basis on early studies disregarding the relevance of the coloileal reflux; and incomplete knowledge, because up to this moment there are not sufficient studies establishing its relationship with disease or specific clinical manifestation. Both reasons are questionable, requiring more reflection. After all, if in the rest of the whole digestive tract the refluxes play a clear and frequently health-harmful role^(4,5), why would only the coloileal reflux be an exception, or, why would it not have a relevant meaning? Let us consider, for example, a real situation in which the barium enema identifies an intense coloileal reflux, with a high potential capacity of transferring large amounts of bacteria to the small intestine, along time. We assume that such a reflux could generate the conditions required for the small intestine contamination with anaerobe flora and the establishment of the bacterial overgrowth syndrome with metabolic and nutritional effects. This hypothesis is favored by several studies demonstrating that resection and other conditions sacrificing the CIJ integrity result in intestinal contamination^{(15,17,18,31)}.

Although attractive, all these conjectures fail to be confirmed due the scarcity of data regarding different basic aspects of the coloileal reflux. For example, which is its prevalence at barium enema? Which would the intensity variation be? Which type of population would be affected? Men? Women? Youngsters? Elders? Insufficient information and the absence of answers to the above questions have encouraged us to develop the present study with the purpose of verifying the coloileal reflux prevalence in barium enemas, classifying its intensity grade and determining the sex and age of the population affected.

MATERIALS AND METHODS

Radiologic reports of 715 consecutive barium enemas performed in the last two years at the Imaging Diagnosis Service of the Clinics Hospital, Faculdade de Medicina de Botucatu-Unesp, were reviewed, corresponding to 268 male and 447 female patients, with an average age of 54 years (ranging from 14 to 93 years). Indications for the enemas were diverse, so they were not directed to specific conditions.

The performance of the barium enema was based on the Fischer-Wellin technique, with patients complying to the following schedule: the day before the test, low-residue diet and laxative administration in the evening; at the day of the procedure, fast observation; the patients were then submitted to intestinal washing to complete the large intestine cleaning and after that were taken to the examination room, where they received a variable volume barium sulphate at 50% rectal infusion, sufficient to reach the transverse colon. Following that, postural maneuvers were performed to fill the segment between the colon and the cecum. After this, the patient was asked to evacuate the contrast and come back to the radiologic table where the test was completed with air pumping into the colon, with the purpose of obtaining double contrast intestine images.

The analysis of the radiologic test and later report elaboration was made, at least, by two radiologists previously oriented to research and characterize the existence of contrast reflux into the terminal ileum. According to our previous study, the coloileal reflux was classified into four categories: absent, mild, moderate and severe⁽³²⁾. One considered the mild coloileal refluxes those of subtle aspect, characterized by rapid visualization of a small volume of contrast penetrating into the ileum and rapidly emptied from it; moderate, the well evidenced reflux remaining in the ileum along the examination and ascending up to the terminal 20cm of the ileal loop; severe, the great refluxes exceeding the ileum distal 20 cm, sometimes reaching the jejunum and remaining retained during the examination.

RESULTS

Of the total 715 enemas reviewed, 333 (46.5%) presented coloileal reflux, rated as mild in 150 (45%), moderate in 125 (37.5%) and severe in 58 (17.5%) (Figures 1, 2 and 3).

Of the 447 women studied, 216 (48.3%) presented coloileal reflux, rated as mild in 102 (47.2%), moderate in 75 (34.8%) and severe in 39 (18%), while of the 268 men investigated, the coloileal reflux was present in 117 (43.6%), rated as mild in 48 (41%), moderate in 50 (42.7%) and severe in 19 (16.3%). The distribution by sex and respective grades is shown in the Table 1.

As to the age range, the coloileal reflux was observed in six (46.1%) of 13 patients bellow 21 years of age, in 54 (42.1%) of 128 patients between 21 and 40 years, in 157 (49.8%) of 315 patients between 41 and 60 years and in 116 (44.7%) of 259 patients more than 60 years old. The distribution by age and grades can be seen in the Table 2.

DISCUSSION

The developed study has allowed us to analyze a comprehensive sample. Although it is not possible to completely extrapolate the results to the general population due to ethical restrictions, the comprehensiveness of the sample regarding the individuals sex and age and the variety of indications resulting from the barium enemas reviewed guarantee a material with reasonable representativeness allowing the establishment of consistent initial fundamentals for a better understanding of the coloileal reflux. Additionally, the criterion of choosing the cases on a consecutive basis during a two-year continuous period, maintaining a involved team composition stability and the uniformity of the radiological technique employed, contribute to the assurance of a high reliability of encountered results.

The results analysis firstly has showed that 46.5% (333 individuals) of the studied population presented coloileal reflux. Almost a half of these cases (45%) presented a mild, transitory reflux with an inexpressive volume. The remaining 55%, or 183 cases, presented well evidenced reflux, with marked intensity, being 68% included in the moderate category and 32% included in the severe category. These findings have led us to the conclusion that the coloileal reflux prevalence is significant, since almost half of the 715 cases reviewed presented reflux, with 55% of these cases with well defined features and considerable volume.

With regards to the sexual prevalence (Table 1), the reflux was present in 48,3% of the women and in 43.6% of the men, suggesting a reduced influence of gender on the coloileal reflux occurrence. When considering its grade, it was possible to observe a discreet predominance of women over men with mild reflux and a disadvantage in the moderate reflux. These differences, however, have not reached values that could suggest higher severity of the refluxes in men than those in women.

About the possible influence of the age range on the coloileal reflux frequency (Table 2), it is important to mention that, despite the great difference in the number of individual less than 21 years old (13 individuals) compared to the number of individuals in other age groups, even in this group the proportion of cases with reflux was quite close to that presented by the other age groups, suggesting a similarity of coloileal reflux frequency, about 45%, regardless of patients age. This differentiates the coloileal reflux from the other intestinal conditions like diverticular disease or cancer where there is a clear predominance in age ranges above 50 years. When the analysis was based on the disease grade, we could observe a discreet predominance of moderate and severe grades in the age group above 60 years, when compared to lower age ranges.

The presence of coloileal reflux leads to two relevant questions: the first one, of etiopathogenic character % why would the reflux occur? The second one, of practical character % is it possible that this occurrence is related not only to the sphincteric function disorders, like hypotonia, but also to anatomical defects as those described in papers of Kumar & Phillips⁽²⁶⁾ and Kumar et al.⁽²⁷⁾, demonstrating the relevance of the integrity of ileocecal ligaments and of the ileocecal acute angulation for the ileocecal junction (ICJ) competence preservation?

With regards to the reflux consequences, some studies have showed that the ileocecal valve alteration, due to an intrinsic disease or surgical intervention, causes changes in the ileal motility and favors the small intestine contamination by the colon bacteria^{(15,17,18,33,34)}. Although the coloileal reflux causal mechanisms diagnosed in the present study are yet to be known, we can assume that the patients affected are individuals with a higher potential to develop ileal motility disorders and small intestine contamination, with possible and different clinical manifestations as a result^{(15,16,31,35)}.

As a conclusion, in the reviewed barium enemas, our study has found a moderate and severe coloileal refluxes prevalence of approximately 25%, without an evident association with sex or age range. Although this reflux effects are unknown, among the foreseeable consequences we can include the distal small intestines bacterial contamination and the appearance of ileal motility alterations.

REFERENCES

Received March 24, 2005.

Accepted after revision July 1st, 2005.

• 1. DiDio LJA, Anderson MC. The "sphincters" of the digestive system. Baltimore, MD: Williams & Wilkins, 1968.
• 2. Vaezi MF, Richter JE. Diagnosis and management of achalasia. Am J Gastroenterol 1999;94:34063412.
• 3. Spechler SJ, Castell DO. Classification of oesophageal motility abnormalities. Gut 2001;49:145151.
• 4. Dent J, Holloway RH, Toouli J, Dodds WJ. Mechanisms of lower oesophageal sphincter incompetence in patients with symptomatic gastrooesophageal reflux. Gut 1988;29:10201028.
• 5. Dodds WJ, Dent J, Hogan WJ, Helm JF, Hauser R, Patel GK. Mechanisms of gastroesophageal reflux in patients with reflux esophagitis. N Engl J Med 1982;307:15471552.
• 6. Cheung O, Wald A. Review article: the management of pelvic floor disorders. Aliment Pharmacol Ther 2004;19:481495.
• 7. Rao SSC. Pathophysiology of adult fecal incontinence. Gastroenterology 2004;126:S14S22.
• 8. Becker JM. Physiology of motor function of the sphincter of Oddi. Surg Clin North Am 1993;73: 12911309.
• 9. Kalloo AN, Pasricha PJ. Therapy of sphincter of Oddi dysfunction. Gastrointest Endosc Clin N Am 1996;6:117125.
• 10. Weisbrodt NW. Motility of the small intestine. In: Johnson LR, editor. Physiology of the gastrointestinal tract. 2nd ed. New York, NY: Raven Press, 1987;631663.
• 11. Bellón Carneiro JM, Jiménez MF, Oliveros LG. El esfínter ileocecal en la dinámica funcional del tracto digestivo: revisión de conjunto. Rev Esp Enf Ap Digest 1987;72:745748.
• 12. Calabuig R, Weems WA, Moody FG. Ileo-cecal junction: a valve or a sphincter? An experimental study in the opossum. Rev Esp Enferm Dig 1996; 88:828839.
• 13. Phillips SF, Quigley EM, Kumar D, Kamath PS. Motility of the ileocolonic junction. Gut 1988;29: 390406.
• 14. Monereo J, Martinez-Almoyna C. Incompetencia de la válvula ileocecal. Rev Esp Enferm Apar Digest 1977;49:467484.
• 15. Li E. Bacterial overgrowth. In: Yamada T, editor. Textbook of gastroenterology. 3rd ed. Philadelphia, PA: Lippincott Williams & Wilkins, 1999;16971708.
• 16. Spiller RC, Brown ML, Phillips SF. Emptying of the terminal ileum in intact humans. Influence of meal residue and ileal motility. Gastroenterology 1987; 92:724729.
• 17. Myrvold H, Tindel MS, Isenberg HD, Stein TA, Scherer J, Wise L. The nipple valve as a sphincter substitute for the ileocecal valve: prevention of bacterial overgrowth in the small bowel. Surgery 1984;96:4247.
• 18. Griffen Jr WO, Richardson JD, Medley ES. Prevention of small bowel contamination by ileocecal valve. South Med J 1971;64:10561058.
• 19. Cohen S, Harris LD, Levitan R. Manometric characteristics of the human ileocecal junctional zone. Gastroenterology 1968;54:7275.
• 20. Kruis W, Phillips S, Zinsmeister A. Flow across the canine ileocolonic junction: role of the ileocolonic sphincter. Am J Physiol 1987;252:G13G18.
• 21. Nasmyth DG, Williams NS. Pressure characteristics of the human ileocecal region a key to its function. Gastroenterology 1985;89:345351.
• 22. Ouyang A, Snape WJ Jr, Cohen S. Myoelectric properties of the cat ileocecal sphincter. Am J Physiol 1981;240:G450G458.
• 23. Miller, RE. Complete reflux small bowel examination. Radiology 1965;84:457463.
• 24. Castellino RA, Verby HD, Friedland GW, Northway WH. Delayed barium aspiration following complete reflux small bowel enema. Br J Radiol 1968; 41:937939.
• 25. Miller RE. Barium-enema examinations with large-bore tubing and drainage. Radiology 1964;82:905911.
• 26. Kumar D, Phillips SF. The contribution of external ligamentous attachments to function of the ileocecal junction. Dis Colon Rectum 1987;30:410416.
• 27. Kumar D, Phillips SF, Brown ML. Reflux from ileum to colon in the dog. Role of external ligamentous attachments. Dig Dis Sci 1988;33:345352.
• 28. Thompson JK, Kochler RE, Richter JE. Detection of gastroesophageal reflux: value of barium studies compared with 24-hr pH monitoring. AJR 1994;162:621626.
• 29. Sellar RJ, De Caestecker JS, Heading RC. Barium radiology: a sensitive test for gastrooesophageal reflux. Clin Radiol 1987;38:303307.
• 30. Chen MYM, Ott DJ, Sinclair JW, Wu WC, Gelfand DW. Gastroesophageal reflux disease: correlation of esophageal pH testing and radiographic findings. Radiology 1992;185:483486.
• 31. King CE, Toskes PP. Small intestine bacterial overgrowth. Gastroenterology 1979;76:10351055.
• 32. Machado WM, Nishimura MR, Nakamura EK, Pola PMS, Morceli J. Refluxo cecoileal (RCI): prevalência e classificação. GED 2000;19(Supl 2):S17.
• 33. Singleton AO, Redmond DC 2nd, McMurray JE. Ileocecal resection and small bowel transit and absorption. Ann Surg 1964;159:690694.
• 34. Fallingborg J, Pedersen P, Jacobsen BA. Small intestinal transit time and intraluminal pH in ileocecal resected patients with Crohn's disease. Dig Dis Sci 1998;43:702705.
• 35. Phillips SF, Camilleri M. The ileocecal area and the irritable bowel syndrome. Gastroenterol Clin North Am 1991;20:297311.

*

Study developed at the Clinics Hospital, Botucatu Faculty of Medicine, Unesp, Botucatu, SP.

Publication Dates

• Publication in this collection
  25 May 2006
• Date of issue
  Apr 2006

History

• Received
  24 Mar 2005
• Accepted
  01 July 2005