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Radiographic studies of duodenum and jejunum in man
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R A D I O G R A P H I C S T U D I E S OF D U O D E N U M JEJUNUM IN MAN
AND
BY DR. J. W. McLAREN, DR. G. M. ARDRAN, AND DR. J. SUTCLIFFE FROM THE NUFFIELD INSTITUTE FOR MEDICAL RESEARCt{~ OXFORD
RADIOLOGISTSin the last decade have shown increasing interest in the pathological appearances of the small intestine. It is unfortunate that the appearances in the normal subject seem to have been somewhat neglected. With this point in mind it was decided to investigate radiographically movements of the duodenum and jejunum in normal subjects. Investigations of the movements of the human alimentary tract have been carried out previously by numerous workers, using widely varying radiological techniques, among whom may be mentioned Groedel (i912), Cole (i934) , Barclay (1936 , i939) , Ross Golden (1945). Extensive work on animals has been performed by Cannon (1911) and Alvarez (194o) and many other workers. The correlation between the findings of animal experiments and the normal human subject is difficult and a problem which has not yet been satisfactorily solved.
METHOD In the following study the method chosen as offering the best means of investigation was that of utilizing direct rapid serial radiography with the use of contrast medium. The apparatus used was that devised by Barclay, Franklin and Prichard (194o). This enabled us to take natural-sized direct films 5 in. square at the rate of 2 per second for a period of 2o seconds. The main advantage of this method is the production of natural-sized films with detail comparable to that seen on standard radiographs. These films can then be copied on to i6-mm, cine films, and projected at a normal speed, and the combined cine projection and 5 in. square films when considered together give a very adequate idea as to the movement and changes taking place in the intestine. T h e drawbacks of the method are : (i) the limited field examined in any one series, and (2) the comparatively short time (20 sec.) over which such studies can be made. T h e relatively slow rate (2 per sec.) at which the films are taken is not a disadvantage as might at first be thought, but has proved advantageous in drawing attention to small degrees of movement. Bowel movements are seldom so rapid that the movements occurring between films cannot be adequately envisaged. The main alternative radiological method is that of 35-ram. indirect photofluorography. The chief advantage of this technique is the large field which can be covered, but detail in individual frames is relatively poor and subsequent analysis of movement and mucosal pattern changes is very difficult. The combination of both methods has not been used in this investigation, but may well prove fruitful in the future.
TECHNIQUE Selection and Preparation of M a t e r i a L - - H e a l t h y medical student volunteers were used and an extensive questionnaire completed to ensure that there was no reason to suppose any digestive or other abnormality. Prior to the examination, which was carried out in the morning, the individual was requested to fast from the previous night. E x a m i n a t i o n . - - E a c h volunteer was given by mouth 4 oz. of barium sulphate mixed to a cream with normal saline. T h e subject was then screened at intervals until the contrast medium was seen to be at the required site and intestinal movements were taking place. The subjects were all prone on a specially devised stretcher which ensured similar conditions of pressure, as far as possible, on the abdominal wall during screening and subsequent radiography. The centre of the area selected to be radiographed was marked with ink under screen observation. T h e area
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chosen was, as far as possible, free of obscuring bowel coils and bony structures. After marking,* the stretcher and subject were rapidly and accurately positioned over the serial radiographic equipment. During the serial radiography the volunteer held his breath in a neutral position after slight
Fig. 2 t 2 . - - I n k marker as designed by the late Dr. A. E. Barclay. I t consists of a metal ring and handle ; on pressing the end (A) an inked wick projects at the centre of the metal rin~ (B) which points in the direction of the patient and marks the skin.
overventilation of the lungs. He had previously been instructed how to carry out this procedure. As a rule no difficulty was experienced in holding the breath for 20 sec. After an interval, other series of films might be taken at the same or different area as required. (Fig. 213. )
I J
Fig. 2 1 3 . - - T o illustrate the position of patient during screening and marking procedures.
Arrow indicates direction of movement of stretcher and patient to centre over serial radiographic apparatus.
M o d e o f A n a l y s i s . - - T h e 5-in. square pictures have been taken serially on a roll of film and after processing the whole strip of about 4 ° pictures can be viewed directly. T o study the movements which have occurred during the serial radiography each 5-in. square film is reduced on to i6-mm, film, and in order that this may be projected at a true rate each frame is copied 8 times, * The marker, devised by Dr. A. E. Barclay, is seen in the diagram (Fig. 212). I0
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On projection (at I6 frames per second) we thus see each serial film projected for half a second. This method produces a slight discontinuity of movement every half second. This is extremely valuable in emphasizing slight movements which might otherwise have passed unnoticed or required
A.--Time
zero
E . - - 2 sec.
B.--½ sec.
F.--2½ sec.
C.--I
G . - - 3 ½ sec.
sec.
D.--1½ see.
H.--4 see.
Fig. 214.--Illustrates non-progressive segmentation in length of jejtmurn.
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Fig. 2 I S . - - D i a g r a m m a t i c "representation of movements depicted in Fig, 214.
A.--Time zero
B . - - ½ sec.
Fig. 216.--Non-progressive segmentation in the duodenum.
C.--2½
sec.
O . - - 5 sec.
T h i s also illustrates the presence of the so-called ' cap sphincter '.
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considerable detailed analysis to detect. Each series of approximately 4 ° radiographs is thus converted into a strip of i 6 - m m , film containing 32o frames. This is spliced to produce a loop which can be projected contitmously and so allow prolonged study. While most of the movements can be easily seen on the cinematographic record thus obtained, it i s often of considerable value to refer
A . - - T i m e zero
B.--½ sec.
"Fig. zi7.--Another example of non-progressive segmentation in the duodenum.
C . - - I sec.
D.--1½ sec.
The ' c a p sphincter' is again noted.
back to the natural-sized films for details of movements which may show more readily especially when combined with mucosal detail. Frequently the air contained in the bowel has been shown well enough to be able to see that the movements appear to be the same as with the bowel outlined with contrast medium. Quantity of M a t e r i a L - - C o n c l u s i o n s reached in this work have been derived from a study of over 3 ° volunteers, involving over ioo examinations. W o r k on these lines is still proceeding, and each fresh case to date has failed to alter the conclusions reached on the first series.
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Each series of films when made into a loop as described above requires a considerable time for analysis. It is impossible in most cases to envisage completely the movements occurring without repeated observation of each patch of barium projected on the screen. The amount of labour involved in analysing over IOO examinations is very considerable.
A . - - T i m e zero
B . - - 2 ½ sec.
C.--8½ sec.
D . - - 1 3 sec.
Fzg. 2 I S . - - T h e s e are selected frames from the series showing progressive segmentation in the jejunum.
This figure also
illustrates ' accommodation ' between adjacent loops of bowel.
Investigation of Pathological Cases.--This paper is not concerned with subjects other than those believed to be normal. Work is, however, proceeding using pathological material, and useful information with regard to altered motility, etc., of the bowel has been obtained. Dose of Radiation received by the Volunteers.--Observations have been carried out and the total amount of radiation received by the subject for each series of films is of the order
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of IO r. The work has been carried out at 27-in. focus-film distance, u s i n g 2 mm. of aluminium filtration above the inherent filtration of the tube. A cone is used which accurately confines the primary beam to a square not greater than 5~ in. at film level. Thus the total area irradiated and
A.--Time zero
C.--2
sec.
B . - - I sec.
D.--2½
sec,
the total dose received is comparatively small. No subject has received a total dose of more than 5° r. F u r t h e r O b s e r v a t i o n s o n t h e M e t h o d . - - T h e method as outlined above demonstrates the bowel lumen and mucosal folds, and movements are indicated both by the bodily transfer of barium through the bowel lumen and by the changing pattern of the mucosal folds. Invariably it is observed that the mucosal folds point in the direction of flow, though whether this is because they are passively dragged in this direction by the moving contents or whether they are actively moved by contractions of the muscularis mucos~e as described by Forssell, is not certain.
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It will be seen from the illustrations that even the smallest fleck of barium may be followed in its movements in the bowel, and that it is possible to study the alterations occurring in a single mucosal fold particularly in the duodenum and upper jejunal region.
E . - - 3 sec.
G . - - 5 sec.
F . - - 4 see.
H.--7
sec.
Fig. a I 9 . - - T h i s is a series iIlustrating a rush peristaltic movement in the jejunum.
Note also the dragging of the mucosal folds in the direction of movement of barium.
This method appears to us to be that which is the most physiological of all available methods. The main deviations from normal physiology can be attributed to, firstly, the fact that the subject undergoing investigation may be a little apprehensive ; secondly, he is examined after a not very extensive fasting; and, thirdly, that barium may not necessarily cause the bowel to react in the same manner as any given food.
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Other methods applied in man, such as those involving intestinal balloons, etc., are obviously unphysiological, and appearances observed under anaesthesia may well be abnormal. Observations in animals are complicated by the effects of anmsthesia and operative procedures--X-ray barium meal studies in suitably available animals have so far shown complete dissimilarity of the general radiographic appearance when compared with those found in man. The absence of an experimental animal showing similar X-ray appearances has so far foiled attempts to correlate bowel movements as seen in the open abdomen with those observed radiographically. L i m i t a t i o n s . - - B o w e l contents only are shown in our films and these are no direct indication of the form of the contractions of the intestinal musculature responsible for each type o f movement of the contents. T h e terms used in describing various types of movement are for the most part those which have come into general use in the past. These terms have sometimes been used to describe contractions of intestinal muscle and sometimes to describe movements of intestinal contents. Until a method is devised whereby contractions of muscle and movements of contents can be simultaneously recorded, the use of descriptive terms in this way may involve some discrepancy. This applies to the present investigation. Each portion of intestine, however, presents such a detailed, delicate, and distinctive pattern, that it seems likely that a particular form of contraction of the intestinal wall will produce a characteristic change in pattern of the contents, and, further, that motionless contents indicate a quiescent musculature, i.e., no significant contractions can occur without leaving their record in the films, provided that the lumen is completely filled with contrast medium, or that the mucosa is outlined.
GENERAL APPEARANCES When the small intestine is observed in a subject who has ingested barium it is seen that the barium may not be evenly distributed throughout the bowel but is localized in uneven lengths. If a short length containing barium is observed the barium may either be in a more or less continuous column or may be split up into separate masses. The mucosa in intervening portions is usually rendered just visible by a very thin coating of barium adhering to it. In these areas the mucosa, which is coated with barium between barium masses, may be seen to be either in actual constriction or to be in a flaccid condition. Non=Progressive Segmentation.--Periodically, in a barium-filled portion of bowel one observes a constriction, at right angles to the long axis of the bowel, which squeezes the barium to either side. The constriction is localized and ring-like, but widens to a varying degree orally and caudally to i-2 cm. It is assumed that this constriction is caused by a contraction of circular muscle-fibres in this region. This type of contraction may be isolated or may be one of a series of similar contractions occurring fairly close together. The movement observed when this type of contraction occurs is described in future as non-progressive segmentation. After an interval a similar process may take place in that portion of bowel into which the barium was squeezed by the previous contraction, thus returning the barium largely to its original situation. When non-progressive segmentations are occurring close together in a length of intestine the caudally squeezed mass from one contraction usually unites with the orally squeezed mass of adjacent contraction, forming a fresh mass. After an interval the ne:~t contraction usually occurs near the middle of a re-formed b a r i u m mass, splitting it and returning the barium to its initial site. (Figs. 214-217). Progressive S e g m e n t a t i o n . - - I n the description of non-progressive segmentation the barium filling a portion of bowel would be divided and squeezed in opposite directions in approximately equal amounts over a fair length, later being returned more or less to its original site. Should the masses of barium be of unequal size or the ring contraction spread more one way than the other, then progressive segmentation has occurred. As a general rule the larger of these masses will
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again be segmented unequally, the main mass progressing in the same direction as that of the initial contraction (Fig. 218). By this means a mass may move fairly rapidly along a length of bowel. In most instances progressive segmentation only occurs caudally, but quite frequently, especially in the duodenum, the orally moving and usually smaller mass may progress a considerable way. Throughout the second part of the duodenum where it is easily observed, and to a lesser extent in the jejunum, there is a process which appears to be quite definitely a type of ' scavenging '
A . - - T i m e zero
C . - - 7 sec.
B.--3½ sec.
D . - - 8 ½ sec.
Fig. 2 2 o . - - I l l u s t r a t e s ' cap s p h i n c t e r ' a n d m u c o s a l p a t t e r n o f d u o d e n u m , p a r t i c u l a r l y at t h e a p e x of t h e cap.
mechanism, as happens when the main mass of barium has progressed caudally by a segmental movement and the remaining part of the barium is gathered up by a smaller and succeeding progressive segmental contraction. R u s h P e r i s t a l s i s . - - F r e q u e n t l y one observes a mass of barium which travels rapidly through several loops of intestine. This movement is commonly initiated by a progressive segmentation, but once started seems to be actively propelled, rather than merely ' squeezed ', and travels much farther than when occurring in a simple progressive segmentation without appearing to come to rest. In this case the intestine preceding the mass appears to be in a state of relaxation without dilatation. The appearance of the mucosa following passage of the barium mass, though dragged and pointing in the direction of the movement, seems to indicate that the bowel is not actively
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constricted but may even be flaccid. At the end of a rush there is often a degree of reverse peristalsis seen; this may be not well shown but in some instances may be fairly noticeable (Fig. 219). Ring G o n s t r i c t i o n s . - - I n a column of barium it has been observed that a localized constriction can occur indicating a ring constriction at this point. This may be complete or incomplete. T h e constriction of the barium column is narrow and there is no indication that the contraction spreads to either side and there is minimal displacement of barium. This has been observed concurrently with the segmental movements previously described. The partial ring contraction
A , - - T i m e zero
B.--"
sec.
C . - - I sec.
D.--1½
sec.
Fig. 2 z i . - - I l l u s t r a t e s reflux from the second part of the d u o d e n u m into the duodenal cap.
may be superimposed on the segmental movement without obviously affecting each other. The incomplete ring contractions are merely incisural indentations of the barium column and are transient. It is of interest to note that these have been seen in the duodenal cap. Pendnlar M o v e m e n t s . - - T h e r e is considerable doubt as "to what is really meant by pendular movements. Some modern text-books describe pendular movements as the side-to-side swaying movements of individual loops of intestine. They are probably a consequence of movement in adjacent portions of bowel. Other authors' descriptions of pendular movements appear identical with what we have described as 'non-progressive segmentation '. T h e y describe these movements as simple annular constrictions travelling up and down short lengths of the bowel in a to-andfro fashion. In our films we have not conclusively demonstrated the first type of so-called pendular movement, probably because of the small area and short duration of the examination.
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O t h e r M o v e m e n t s . - - S o m e t i m e s changes in calibre are noted in the barium mass outlining a well-filled loop of intestine, without any actual movement of b a r i u m or evidence of the above types of contraction. T h i s probably represents an ' accommodation ' of the bowel to movements elsewhere, and may possibly represent the results of the first type of pendular movement or may indicate a change in tone of bowel (Fig. 218). ' T h e C a p S p h i n c t e r ' . - - T h e part of the duodenum immediately distal to the cap appears to function as a ' s p h i n c t e r ' even though there is no anatomical sphincter in this region. T h i s functional sphincteric action is seen under several circumstances. It is quite frequent to find that there is a small area devoid of barium, between the barium within the cap and that in the
A.--Time
zero
B.--10 sec.
~
C.--13½
D.--20
sec.
sec.
Fig. 2 2 2 . - - A series showing the formation and disappearance of an incisural notch in the base of the duodenal cap.
main part of the duodenum. This band is maintained in the presence of active moulding contractions of the cap which alter its shape and apparent size when there has been no flow of barium either into or out of the cap in either direction. W h e n a wave of gastric peristalsis drives barium onward through the cap to the second part of the duodenum a constriction appears, frequently leaving the cap filled with a clear area distal to it. This separates it from the main mass, which continues down the second part of the duodenum (Fig. 220). I n a similar way it is quite frequent to see a small mass of b a r i u m passing back into the second part of the duodenum as far as this ' s p h i n c t e r '. I n some cases after a temporary hold-up this ' s p h i n c t e r ' relaxes and allows the barium to pass back into tile cap (Fig. 221). This phenomenon m a y be seen where there is a reverse peristalsis of a whole mass of barium or may be due to the reverse movements seen in the tail of a ' non-progressive segmentation '
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D u o d e n a l C a p . - - T h e mode of filling of the duodenal cap has been shown to be varied. As previously mentioned, this cap, while remaining full, can alter considerably in shape. This appears to be due to the pyloric sphincter being closed and ' sphincteric ' action distal to the apex of the cap also taking part. The cap appears to try to contract and expel its contents, changing
A . - - T i m e zero
B . - - I sec.
C.--1½
sec.
D.--2
sec.
shape considerably while doing so. It has also been observed that there is occasionally formation of an incisural notch in the basal part of the cap which later completely relaxes (Fig. 222). At other times it has been observed that while contracting the duodenal cap shows a very marked longitudinal mucosal pattern which may persist after the main mass of the barium has passed from the cap into the second part. The mucosal markings may persist through the apex of the cap, or blend with the mucosa of the second part of the duodenum, or may be nipped off by the ' sphincter '. In some examples we have observed definite movements of barium from the cap back into the stomach.
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D u o d e n u m . - - I n the duodenum we have observed the following types of movement as described in detail above: (i) Non-progressive segmentation; (2) Progressive segmentation; (3) Rush peristalsis ; (4) Ring contraction. Pendular movements of the first type to be described have not been noted.
E.--3 see.
F.--3~ sec.
G . - - 5 sec.
H . ' 5 ½ sec.
Fig. 2 2 3 . - - T t l i s series illustrates the change in rnueosal pattern in the second part of the duodenum.
T h e mucosal p a t t e r n changes from a feathery to a ' pavement ' type and changes again to the feathery state.
Progressive segmentation with the main mass moving orally has been noted more frequently in the duodenum than in the jejunum. Because of its lack of mesentery the duodenum is more fixed than the jejunum, and when initially filled is unobscured by the barium in other loops of intestine. For these reasons, and also because the main part of the duodenum is parallel to the film, we have been able to note mucosal changes readily. We have noticed on several occasions that the mucosal pattern can change comparatively rapidly. For instance, in several cases we
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have seen that the mucosal pattern is predominantly transverse and can change during a few frames to a ' pavement ' type. This may last for a second or two and then change back again. These changes have been noted when there has been no gross movement of barium in the duodenum while the mucosa only has been just outlined (Figs. 223, 224).
A.--Time
zero
B . - - 2 sec.
C . - - 3 sec.
D . - - 6 sec.
J e j u n u m . - - A l l the main types of movements that have been seen in the duodenum are visualized in the j e j u n u m with the exception that we have not observed anything comparable to a localized sphincteric action such as we have seen in the duodenum. Progressive segmentation in the predominantly oral direction is considerably less common than in the duodenum. While in the duodenum it has been noted that the actual mucosal pattern can change very considerably in a short interval, this has not been observed in the jejunum ; but in the jejunum the mucosa seems to be very greatly influenced by bowel movement in that the mucosa gives an impression of being more loosely attached to the muscular coat and is therefore more susceptible to movement of the bowel contents.
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Rate of Bowel Movement and Mucosal Pattern Changes.--The following examples of rates of different types of movement are only given in very approximate figures. No corrections have been made for distance of the bowel from the film, magnification due to short focus-film distance (27 in.), or obliquity of the direction of the bowel. In many instances during the 2o-second
E.--8½ sec.
F.--13 sec.
G.--15½
sec.
H . - - 1 7 sec.
Fig. 224.--A typical duodenal series including filling and emptying of the cap and segmental movement in the second part.
period when the film is being exposed practically no movements can be noted. At other times one observes on the screen movements which are extremely rapid and of such short duration that no time is allowed for positioning the patient and making an exposure. Movements in the jejunum appear to be much more variable in their rate than those in the duodenum. Subject to the above limitations some examples are now given of rates of the different types of movement : - -
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I. Non-progressive Segmentation.--The time taken for a mass of barium to be segmented and return to approximately its original position is of the order of 4 seconds. 2. Progressive Segmentation.--From the commencement of the contraction segmenting a mass of barium to its arrival at a point where it remains stationary before being re-segmented, has been noted as being between 3"5 and 6 seconds. T h e distance travelled is of t h e order of i o cm. 3. Rush Peristalsis.--In the few examples of rush peristalsis that we have managed to record, the rate of travel has been approximately 60 cm. in 12 seconds. This estimation is probably open to even greater inaccuracy than the previous one, since it is inevitable that, the barium mass having travelled through several coils, the measurements can only be estimated approximately when only barium content can be visualized. 4. Ring Contractions.--Ring contractions have been observed to appear and disappear in 3½ seconds. Incisural notch formation or partial ring contraction has been Observed to appear in 4 seconds, persist for 4 seconds, and disappear in 4 seconds. 5. Intrinsic Mucosal Pattern Change.--In the second part of the duodenum the nmcosa has been observed to change from a ' pavement ' type to a feathery type in about ½ second, stay in the feathery formation for 2 seconds, and return to a ' p a v e m e n t ' type in ½ second. COMMENT
It is realized that the points covered in this article form only a brief survey of a very complicated process. T h e points we have brought out are a few of the more striking things we have noticed after surveying all the variations as seen on the film projections of these studies. We would like to point out that the complexity and wide variation of types of movement and pattern are considerable, and that it is not until prolonged study by a method such as the one described that even an elementary understanding of the screen appearances of bowel movements can be arrived at. W i t h o u t study by this method it is difficult to assess individual radiographs and to have full comprehension of the types of movement, etc., which have produced this appearance. It would seem that the careful study of a series of films showing the normal and its wide variation of movement and pattern must be of considerable value to those workers interested in the normal physiology of the bowel and to those who are interested in assessing the early pathological changes which may be found. :
SUMMARY
A method of serial radiography at the rate of 2 frames per second of the barium-outlined small bowel has been described, together with a combined method of analysis b y cinematography. A brief survey has been made of the types of normal movement found in the duodenum and j e j u n u m and comment made on the mucosal pattern changes. BIBLIOGRAPHY ALVAREZ,W. C. (I94O), The Introduction to Gastroenterology. New York : Paul B. Hoeber. BARCLAY, A. E. (1936), The Digestive Tract. Cambridge University Press. - - - - (I939), Radiology, 33, I7O. - - --FRANKLIN, K. J., and PRICHARD,M. M. L. (I94o), Brit. J. Ra'diol., 13, 227. CANNON, W. B. (I9II), The Mechanical Factors of Digestion, 227. London : E. Arnold. COLE, L. G., and others (1934) , Radiologlc Exploration of the Mueosa of the Gastro Intestinal Tract. St. Paul and Minneapolis: Bruce Publishing Company. GOLDEN, ROSS (I945), Radiologic Examination of the Small Intestine. Philadelphia : J. B. Lippincott Co. GROEDEL, F. M. (1912), Fortschr. R~ntgenstr., Suppl., 27. McLAREN, J. W., and ARDRAN,G. M. (I950), Radiographic Studies of the Duodenum and Jejunum in Man (i6-mm. cine film). London: Science Films Ltd.
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R A D I O G R A P H I C S T U D I E S OF D U O D E N U M JEJUNUM IN MAN
AND
BY DR. J. W. McLAREN, DR. G. M. ARDRAN, AND DR. J. SUTCLIFFE FROM THE NUFFIELD INSTITUTE FOR MEDICAL RESEARCt{~ OXFORD
RADIOLOGISTSin the last decade have shown increasing interest in the pathological appearances of the small intestine. It is unfortunate that the appearances in the normal subject seem to have been somewhat neglected. With this point in mind it was decided to investigate radiographically movements of the duodenum and jejunum in normal subjects. Investigations of the movements of the human alimentary tract have been carried out previously by numerous workers, using widely varying radiological techniques, among whom may be mentioned Groedel (i912), Cole (i934) , Barclay (1936 , i939) , Ross Golden (1945). Extensive work on animals has been performed by Cannon (1911) and Alvarez (194o) and many other workers. The correlation between the findings of animal experiments and the normal human subject is difficult and a problem which has not yet been satisfactorily solved.
METHOD In the following study the method chosen as offering the best means of investigation was that of utilizing direct rapid serial radiography with the use of contrast medium. The apparatus used was that devised by Barclay, Franklin and Prichard (194o). This enabled us to take natural-sized direct films 5 in. square at the rate of 2 per second for a period of 2o seconds. The main advantage of this method is the production of natural-sized films with detail comparable to that seen on standard radiographs. These films can then be copied on to i6-mm, cine films, and projected at a normal speed, and the combined cine projection and 5 in. square films when considered together give a very adequate idea as to the movement and changes taking place in the intestine. T h e drawbacks of the method are : (i) the limited field examined in any one series, and (2) the comparatively short time (20 sec.) over which such studies can be made. T h e relatively slow rate (2 per sec.) at which the films are taken is not a disadvantage as might at first be thought, but has proved advantageous in drawing attention to small degrees of movement. Bowel movements are seldom so rapid that the movements occurring between films cannot be adequately envisaged. The main alternative radiological method is that of 35-ram. indirect photofluorography. The chief advantage of this technique is the large field which can be covered, but detail in individual frames is relatively poor and subsequent analysis of movement and mucosal pattern changes is very difficult. The combination of both methods has not been used in this investigation, but may well prove fruitful in the future.
TECHNIQUE Selection and Preparation of M a t e r i a L - - H e a l t h y medical student volunteers were used and an extensive questionnaire completed to ensure that there was no reason to suppose any digestive or other abnormality. Prior to the examination, which was carried out in the morning, the individual was requested to fast from the previous night. E x a m i n a t i o n . - - E a c h volunteer was given by mouth 4 oz. of barium sulphate mixed to a cream with normal saline. T h e subject was then screened at intervals until the contrast medium was seen to be at the required site and intestinal movements were taking place. The subjects were all prone on a specially devised stretcher which ensured similar conditions of pressure, as far as possible, on the abdominal wall during screening and subsequent radiography. The centre of the area selected to be radiographed was marked with ink under screen observation. T h e area
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chosen was, as far as possible, free of obscuring bowel coils and bony structures. After marking,* the stretcher and subject were rapidly and accurately positioned over the serial radiographic equipment. During the serial radiography the volunteer held his breath in a neutral position after slight
Fig. 2 t 2 . - - I n k marker as designed by the late Dr. A. E. Barclay. I t consists of a metal ring and handle ; on pressing the end (A) an inked wick projects at the centre of the metal rin~ (B) which points in the direction of the patient and marks the skin.
overventilation of the lungs. He had previously been instructed how to carry out this procedure. As a rule no difficulty was experienced in holding the breath for 20 sec. After an interval, other series of films might be taken at the same or different area as required. (Fig. 213. )
I J
Fig. 2 1 3 . - - T o illustrate the position of patient during screening and marking procedures.
Arrow indicates direction of movement of stretcher and patient to centre over serial radiographic apparatus.
M o d e o f A n a l y s i s . - - T h e 5-in. square pictures have been taken serially on a roll of film and after processing the whole strip of about 4 ° pictures can be viewed directly. T o study the movements which have occurred during the serial radiography each 5-in. square film is reduced on to i6-mm, film, and in order that this may be projected at a true rate each frame is copied 8 times, * The marker, devised by Dr. A. E. Barclay, is seen in the diagram (Fig. 212). I0
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On projection (at I6 frames per second) we thus see each serial film projected for half a second. This method produces a slight discontinuity of movement every half second. This is extremely valuable in emphasizing slight movements which might otherwise have passed unnoticed or required
A.--Time
zero
E . - - 2 sec.
B.--½ sec.
F.--2½ sec.
C.--I
G . - - 3 ½ sec.
sec.
D.--1½ see.
H.--4 see.
Fig. 214.--Illustrates non-progressive segmentation in length of jejtmurn.
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Fig. 2 I S . - - D i a g r a m m a t i c "representation of movements depicted in Fig, 214.
A.--Time zero
B . - - ½ sec.
Fig. 216.--Non-progressive segmentation in the duodenum.
C.--2½
sec.
O . - - 5 sec.
T h i s also illustrates the presence of the so-called ' cap sphincter '.
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considerable detailed analysis to detect. Each series of approximately 4 ° radiographs is thus converted into a strip of i 6 - m m , film containing 32o frames. This is spliced to produce a loop which can be projected contitmously and so allow prolonged study. While most of the movements can be easily seen on the cinematographic record thus obtained, it i s often of considerable value to refer
A . - - T i m e zero
B.--½ sec.
"Fig. zi7.--Another example of non-progressive segmentation in the duodenum.
C . - - I sec.
D.--1½ sec.
The ' c a p sphincter' is again noted.
back to the natural-sized films for details of movements which may show more readily especially when combined with mucosal detail. Frequently the air contained in the bowel has been shown well enough to be able to see that the movements appear to be the same as with the bowel outlined with contrast medium. Quantity of M a t e r i a L - - C o n c l u s i o n s reached in this work have been derived from a study of over 3 ° volunteers, involving over ioo examinations. W o r k on these lines is still proceeding, and each fresh case to date has failed to alter the conclusions reached on the first series.
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Each series of films when made into a loop as described above requires a considerable time for analysis. It is impossible in most cases to envisage completely the movements occurring without repeated observation of each patch of barium projected on the screen. The amount of labour involved in analysing over IOO examinations is very considerable.
A . - - T i m e zero
B . - - 2 ½ sec.
C.--8½ sec.
D . - - 1 3 sec.
Fzg. 2 I S . - - T h e s e are selected frames from the series showing progressive segmentation in the jejunum.
This figure also
illustrates ' accommodation ' between adjacent loops of bowel.
Investigation of Pathological Cases.--This paper is not concerned with subjects other than those believed to be normal. Work is, however, proceeding using pathological material, and useful information with regard to altered motility, etc., of the bowel has been obtained. Dose of Radiation received by the Volunteers.--Observations have been carried out and the total amount of radiation received by the subject for each series of films is of the order
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of IO r. The work has been carried out at 27-in. focus-film distance, u s i n g 2 mm. of aluminium filtration above the inherent filtration of the tube. A cone is used which accurately confines the primary beam to a square not greater than 5~ in. at film level. Thus the total area irradiated and
A.--Time zero
C.--2
sec.
B . - - I sec.
D.--2½
sec,
the total dose received is comparatively small. No subject has received a total dose of more than 5° r. F u r t h e r O b s e r v a t i o n s o n t h e M e t h o d . - - T h e method as outlined above demonstrates the bowel lumen and mucosal folds, and movements are indicated both by the bodily transfer of barium through the bowel lumen and by the changing pattern of the mucosal folds. Invariably it is observed that the mucosal folds point in the direction of flow, though whether this is because they are passively dragged in this direction by the moving contents or whether they are actively moved by contractions of the muscularis mucos~e as described by Forssell, is not certain.
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It will be seen from the illustrations that even the smallest fleck of barium may be followed in its movements in the bowel, and that it is possible to study the alterations occurring in a single mucosal fold particularly in the duodenum and upper jejunal region.
E . - - 3 sec.
G . - - 5 sec.
F . - - 4 see.
H.--7
sec.
Fig. a I 9 . - - T h i s is a series iIlustrating a rush peristaltic movement in the jejunum.
Note also the dragging of the mucosal folds in the direction of movement of barium.
This method appears to us to be that which is the most physiological of all available methods. The main deviations from normal physiology can be attributed to, firstly, the fact that the subject undergoing investigation may be a little apprehensive ; secondly, he is examined after a not very extensive fasting; and, thirdly, that barium may not necessarily cause the bowel to react in the same manner as any given food.
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Other methods applied in man, such as those involving intestinal balloons, etc., are obviously unphysiological, and appearances observed under anaesthesia may well be abnormal. Observations in animals are complicated by the effects of anmsthesia and operative procedures--X-ray barium meal studies in suitably available animals have so far shown complete dissimilarity of the general radiographic appearance when compared with those found in man. The absence of an experimental animal showing similar X-ray appearances has so far foiled attempts to correlate bowel movements as seen in the open abdomen with those observed radiographically. L i m i t a t i o n s . - - B o w e l contents only are shown in our films and these are no direct indication of the form of the contractions of the intestinal musculature responsible for each type o f movement of the contents. T h e terms used in describing various types of movement are for the most part those which have come into general use in the past. These terms have sometimes been used to describe contractions of intestinal muscle and sometimes to describe movements of intestinal contents. Until a method is devised whereby contractions of muscle and movements of contents can be simultaneously recorded, the use of descriptive terms in this way may involve some discrepancy. This applies to the present investigation. Each portion of intestine, however, presents such a detailed, delicate, and distinctive pattern, that it seems likely that a particular form of contraction of the intestinal wall will produce a characteristic change in pattern of the contents, and, further, that motionless contents indicate a quiescent musculature, i.e., no significant contractions can occur without leaving their record in the films, provided that the lumen is completely filled with contrast medium, or that the mucosa is outlined.
GENERAL APPEARANCES When the small intestine is observed in a subject who has ingested barium it is seen that the barium may not be evenly distributed throughout the bowel but is localized in uneven lengths. If a short length containing barium is observed the barium may either be in a more or less continuous column or may be split up into separate masses. The mucosa in intervening portions is usually rendered just visible by a very thin coating of barium adhering to it. In these areas the mucosa, which is coated with barium between barium masses, may be seen to be either in actual constriction or to be in a flaccid condition. Non=Progressive Segmentation.--Periodically, in a barium-filled portion of bowel one observes a constriction, at right angles to the long axis of the bowel, which squeezes the barium to either side. The constriction is localized and ring-like, but widens to a varying degree orally and caudally to i-2 cm. It is assumed that this constriction is caused by a contraction of circular muscle-fibres in this region. This type of contraction may be isolated or may be one of a series of similar contractions occurring fairly close together. The movement observed when this type of contraction occurs is described in future as non-progressive segmentation. After an interval a similar process may take place in that portion of bowel into which the barium was squeezed by the previous contraction, thus returning the barium largely to its original situation. When non-progressive segmentations are occurring close together in a length of intestine the caudally squeezed mass from one contraction usually unites with the orally squeezed mass of adjacent contraction, forming a fresh mass. After an interval the ne:~t contraction usually occurs near the middle of a re-formed b a r i u m mass, splitting it and returning the barium to its initial site. (Figs. 214-217). Progressive S e g m e n t a t i o n . - - I n the description of non-progressive segmentation the barium filling a portion of bowel would be divided and squeezed in opposite directions in approximately equal amounts over a fair length, later being returned more or less to its original site. Should the masses of barium be of unequal size or the ring contraction spread more one way than the other, then progressive segmentation has occurred. As a general rule the larger of these masses will
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again be segmented unequally, the main mass progressing in the same direction as that of the initial contraction (Fig. 218). By this means a mass may move fairly rapidly along a length of bowel. In most instances progressive segmentation only occurs caudally, but quite frequently, especially in the duodenum, the orally moving and usually smaller mass may progress a considerable way. Throughout the second part of the duodenum where it is easily observed, and to a lesser extent in the jejunum, there is a process which appears to be quite definitely a type of ' scavenging '
A . - - T i m e zero
C . - - 7 sec.
B.--3½ sec.
D . - - 8 ½ sec.
Fig. 2 2 o . - - I l l u s t r a t e s ' cap s p h i n c t e r ' a n d m u c o s a l p a t t e r n o f d u o d e n u m , p a r t i c u l a r l y at t h e a p e x of t h e cap.
mechanism, as happens when the main mass of barium has progressed caudally by a segmental movement and the remaining part of the barium is gathered up by a smaller and succeeding progressive segmental contraction. R u s h P e r i s t a l s i s . - - F r e q u e n t l y one observes a mass of barium which travels rapidly through several loops of intestine. This movement is commonly initiated by a progressive segmentation, but once started seems to be actively propelled, rather than merely ' squeezed ', and travels much farther than when occurring in a simple progressive segmentation without appearing to come to rest. In this case the intestine preceding the mass appears to be in a state of relaxation without dilatation. The appearance of the mucosa following passage of the barium mass, though dragged and pointing in the direction of the movement, seems to indicate that the bowel is not actively
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constricted but may even be flaccid. At the end of a rush there is often a degree of reverse peristalsis seen; this may be not well shown but in some instances may be fairly noticeable (Fig. 219). Ring G o n s t r i c t i o n s . - - I n a column of barium it has been observed that a localized constriction can occur indicating a ring constriction at this point. This may be complete or incomplete. T h e constriction of the barium column is narrow and there is no indication that the contraction spreads to either side and there is minimal displacement of barium. This has been observed concurrently with the segmental movements previously described. The partial ring contraction
A , - - T i m e zero
B.--"
sec.
C . - - I sec.
D.--1½
sec.
Fig. 2 z i . - - I l l u s t r a t e s reflux from the second part of the d u o d e n u m into the duodenal cap.
may be superimposed on the segmental movement without obviously affecting each other. The incomplete ring contractions are merely incisural indentations of the barium column and are transient. It is of interest to note that these have been seen in the duodenal cap. Pendnlar M o v e m e n t s . - - T h e r e is considerable doubt as "to what is really meant by pendular movements. Some modern text-books describe pendular movements as the side-to-side swaying movements of individual loops of intestine. They are probably a consequence of movement in adjacent portions of bowel. Other authors' descriptions of pendular movements appear identical with what we have described as 'non-progressive segmentation '. T h e y describe these movements as simple annular constrictions travelling up and down short lengths of the bowel in a to-andfro fashion. In our films we have not conclusively demonstrated the first type of so-called pendular movement, probably because of the small area and short duration of the examination.
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O t h e r M o v e m e n t s . - - S o m e t i m e s changes in calibre are noted in the barium mass outlining a well-filled loop of intestine, without any actual movement of b a r i u m or evidence of the above types of contraction. T h i s probably represents an ' accommodation ' of the bowel to movements elsewhere, and may possibly represent the results of the first type of pendular movement or may indicate a change in tone of bowel (Fig. 218). ' T h e C a p S p h i n c t e r ' . - - T h e part of the duodenum immediately distal to the cap appears to function as a ' s p h i n c t e r ' even though there is no anatomical sphincter in this region. T h i s functional sphincteric action is seen under several circumstances. It is quite frequent to find that there is a small area devoid of barium, between the barium within the cap and that in the
A.--Time
zero
B.--10 sec.
~
C.--13½
D.--20
sec.
sec.
Fig. 2 2 2 . - - A series showing the formation and disappearance of an incisural notch in the base of the duodenal cap.
main part of the duodenum. This band is maintained in the presence of active moulding contractions of the cap which alter its shape and apparent size when there has been no flow of barium either into or out of the cap in either direction. W h e n a wave of gastric peristalsis drives barium onward through the cap to the second part of the duodenum a constriction appears, frequently leaving the cap filled with a clear area distal to it. This separates it from the main mass, which continues down the second part of the duodenum (Fig. 220). I n a similar way it is quite frequent to see a small mass of b a r i u m passing back into the second part of the duodenum as far as this ' s p h i n c t e r '. I n some cases after a temporary hold-up this ' s p h i n c t e r ' relaxes and allows the barium to pass back into tile cap (Fig. 221). This phenomenon m a y be seen where there is a reverse peristalsis of a whole mass of barium or may be due to the reverse movements seen in the tail of a ' non-progressive segmentation '
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D u o d e n a l C a p . - - T h e mode of filling of the duodenal cap has been shown to be varied. As previously mentioned, this cap, while remaining full, can alter considerably in shape. This appears to be due to the pyloric sphincter being closed and ' sphincteric ' action distal to the apex of the cap also taking part. The cap appears to try to contract and expel its contents, changing
A . - - T i m e zero
B . - - I sec.
C.--1½
sec.
D.--2
sec.
shape considerably while doing so. It has also been observed that there is occasionally formation of an incisural notch in the basal part of the cap which later completely relaxes (Fig. 222). At other times it has been observed that while contracting the duodenal cap shows a very marked longitudinal mucosal pattern which may persist after the main mass of the barium has passed from the cap into the second part. The mucosal markings may persist through the apex of the cap, or blend with the mucosa of the second part of the duodenum, or may be nipped off by the ' sphincter '. In some examples we have observed definite movements of barium from the cap back into the stomach.
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D u o d e n u m . - - I n the duodenum we have observed the following types of movement as described in detail above: (i) Non-progressive segmentation; (2) Progressive segmentation; (3) Rush peristalsis ; (4) Ring contraction. Pendular movements of the first type to be described have not been noted.
E.--3 see.
F.--3~ sec.
G . - - 5 sec.
H . ' 5 ½ sec.
Fig. 2 2 3 . - - T t l i s series illustrates the change in rnueosal pattern in the second part of the duodenum.
T h e mucosal p a t t e r n changes from a feathery to a ' pavement ' type and changes again to the feathery state.
Progressive segmentation with the main mass moving orally has been noted more frequently in the duodenum than in the jejunum. Because of its lack of mesentery the duodenum is more fixed than the jejunum, and when initially filled is unobscured by the barium in other loops of intestine. For these reasons, and also because the main part of the duodenum is parallel to the film, we have been able to note mucosal changes readily. We have noticed on several occasions that the mucosal pattern can change comparatively rapidly. For instance, in several cases we
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have seen that the mucosal pattern is predominantly transverse and can change during a few frames to a ' pavement ' type. This may last for a second or two and then change back again. These changes have been noted when there has been no gross movement of barium in the duodenum while the mucosa only has been just outlined (Figs. 223, 224).
A.--Time
zero
B . - - 2 sec.
C . - - 3 sec.
D . - - 6 sec.
J e j u n u m . - - A l l the main types of movements that have been seen in the duodenum are visualized in the j e j u n u m with the exception that we have not observed anything comparable to a localized sphincteric action such as we have seen in the duodenum. Progressive segmentation in the predominantly oral direction is considerably less common than in the duodenum. While in the duodenum it has been noted that the actual mucosal pattern can change very considerably in a short interval, this has not been observed in the jejunum ; but in the jejunum the mucosa seems to be very greatly influenced by bowel movement in that the mucosa gives an impression of being more loosely attached to the muscular coat and is therefore more susceptible to movement of the bowel contents.
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Rate of Bowel Movement and Mucosal Pattern Changes.--The following examples of rates of different types of movement are only given in very approximate figures. No corrections have been made for distance of the bowel from the film, magnification due to short focus-film distance (27 in.), or obliquity of the direction of the bowel. In many instances during the 2o-second
E.--8½ sec.
F.--13 sec.
G.--15½
sec.
H . - - 1 7 sec.
Fig. 224.--A typical duodenal series including filling and emptying of the cap and segmental movement in the second part.
period when the film is being exposed practically no movements can be noted. At other times one observes on the screen movements which are extremely rapid and of such short duration that no time is allowed for positioning the patient and making an exposure. Movements in the jejunum appear to be much more variable in their rate than those in the duodenum. Subject to the above limitations some examples are now given of rates of the different types of movement : - -
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I. Non-progressive Segmentation.--The time taken for a mass of barium to be segmented and return to approximately its original position is of the order of 4 seconds. 2. Progressive Segmentation.--From the commencement of the contraction segmenting a mass of barium to its arrival at a point where it remains stationary before being re-segmented, has been noted as being between 3"5 and 6 seconds. T h e distance travelled is of t h e order of i o cm. 3. Rush Peristalsis.--In the few examples of rush peristalsis that we have managed to record, the rate of travel has been approximately 60 cm. in 12 seconds. This estimation is probably open to even greater inaccuracy than the previous one, since it is inevitable that, the barium mass having travelled through several coils, the measurements can only be estimated approximately when only barium content can be visualized. 4. Ring Contractions.--Ring contractions have been observed to appear and disappear in 3½ seconds. Incisural notch formation or partial ring contraction has been Observed to appear in 4 seconds, persist for 4 seconds, and disappear in 4 seconds. 5. Intrinsic Mucosal Pattern Change.--In the second part of the duodenum the nmcosa has been observed to change from a ' pavement ' type to a feathery type in about ½ second, stay in the feathery formation for 2 seconds, and return to a ' p a v e m e n t ' type in ½ second. COMMENT
It is realized that the points covered in this article form only a brief survey of a very complicated process. T h e points we have brought out are a few of the more striking things we have noticed after surveying all the variations as seen on the film projections of these studies. We would like to point out that the complexity and wide variation of types of movement and pattern are considerable, and that it is not until prolonged study by a method such as the one described that even an elementary understanding of the screen appearances of bowel movements can be arrived at. W i t h o u t study by this method it is difficult to assess individual radiographs and to have full comprehension of the types of movement, etc., which have produced this appearance. It would seem that the careful study of a series of films showing the normal and its wide variation of movement and pattern must be of considerable value to those workers interested in the normal physiology of the bowel and to those who are interested in assessing the early pathological changes which may be found. :
SUMMARY
A method of serial radiography at the rate of 2 frames per second of the barium-outlined small bowel has been described, together with a combined method of analysis b y cinematography. A brief survey has been made of the types of normal movement found in the duodenum and j e j u n u m and comment made on the mucosal pattern changes. BIBLIOGRAPHY ALVAREZ,W. C. (I94O), The Introduction to Gastroenterology. New York : Paul B. Hoeber. BARCLAY, A. E. (1936), The Digestive Tract. Cambridge University Press. - - - - (I939), Radiology, 33, I7O. - - --FRANKLIN, K. J., and PRICHARD,M. M. L. (I94o), Brit. J. Ra'diol., 13, 227. CANNON, W. B. (I9II), The Mechanical Factors of Digestion, 227. London : E. Arnold. COLE, L. G., and others (1934) , Radiologlc Exploration of the Mueosa of the Gastro Intestinal Tract. St. Paul and Minneapolis: Bruce Publishing Company. GOLDEN, ROSS (I945), Radiologic Examination of the Small Intestine. Philadelphia : J. B. Lippincott Co. GROEDEL, F. M. (1912), Fortschr. R~ntgenstr., Suppl., 27. McLAREN, J. W., and ARDRAN,G. M. (I950), Radiographic Studies of the Duodenum and Jejunum in Man (i6-mm. cine film). London: Science Films Ltd.