SOME OBSERVATIONS ON THE TRANSPORT OF FOOD IN THE ALIMENTARY CANAL OF THE RAT Lauri Paloheimo, Aarne Mäkelä and Maija-Liisa Salo Department oj Animal Husbandry , University of Helsinki Received November 2nd, 1953 Definition of the subject and review of earlier investigations Some investigations concerning the transport of food in the alimentary canal of the rat have previously been made in this laboratory (Paloheimo, 9. p. 380—383). Here we have studied 1) the effect of the degree of fullness of the stomach upon its rate of emptying, and 2) the rate of passage of the food in the empty small intestine. Apart from the Paloheimo’s paper (1.c.) we have found only a few publications that deal directly with our present subject. Therefore we shall chiefly refer to papers concerned with the transport of food in man and in animals with a simple stomach other than the rat. According to Scheunert and Trautmax (11, p. 103) the emptying of the stomach in carnivores does not usually begin less than % hour p.c. 1 Krzywanek (5, p. 515), using the x-ray method, observed that in puppies the discharge from the stomach began 30—60 minutes p.c. The pups had received 10—50 g. minced meat. I he filling of the colon began about 4 hours p.c. and the small intestine was empty 7 '2—10 1 2 hours p.c. Magnus (7, p. 227) states that the emptying of the stomach may begin as early as 15 minutes p.c. Stickney et al. (13 p. 399—402) studied, by slaughter tests in dogs, the correlation between the length of the small intestine and the distance (from the pylorus) that an inert test meal traversed in 30 minutes. In dogs with a long small intestine the proportion traversed was 67 % of the length of the small intestine, whereas in dogs with a short small intestine the corresponding figure was 56. In man Rieder (10, p. 464—465), using the x-ray method, observed the contrast gruel in the duodenum immediately after the meal. Fifteen minutes after the test subject had finished a meal consisting of 250 g. of gruel there was contrast material in the ileum, and the stomach was empty 3 14 hours later. The jejunum was dischar- d 4 hours p.c., and the ileum 2 hours later. The experimental meal reached tin p.c. = post cenam = after the meal https://www.c-info.fi/en/info/?token=TnkuHw0v66ErMMIJ.ndKSriq9UtJtRdmz8y87bA.AWbe9MDHzil5_97cxmqA3yakFl1ooXHweyjo75HvCSQv9_TLGDRMnojorWUTV5-LyLNEXlZh-23BkWL5b-GpYeCz4BRydZYhmxOuVSgldZyTnLnOAddhQXZNdmfnvQGVnZUEzTkvrdARj1LFsrpesi5lnbUwOwcfo-CMExdS9_KSoF5FAIjjwC_S8qqFsB9U5ShKNAyhYta6sKsIjy1lu2K0MZc4kUVESeA LAURI PALOHEIMO. AARNE MÄKELÄ AND MAIJA-LIISA SALO caecum 3 hours p.c. Referring to several investigators Schinz, Baensch and Friedi (12, p. 3097) state that 1 y 2 hours p.c. 10—75 % of the food eaten had left the stomach. 1 y 2 hours later the corresponding figure was 30—95, and after a further 1 E hours (4 V 2 hours p.c.) it was 60—90. Nothing is mentioned about the volume of the food portions nor about the method used. The above authors draw attention to some types of especially rapid movements of the small intestine which are distin- guished from the general type of peristaltic movement. They call them Rollbe- wegung or Peristalli sehe Sturz, (ibid. p. 3261). Without indicating the volume of the portions, Swinev and Spurrell (14, p. 43) state that meals that were poor in fat were emptied from the stomach in 2%—3 hours and those rich in fat in 6b, 7 hours. Crider and Thomas (ref. Evans 3, p. 838) 1 state that after large meals the emptying time of the stomach is longer in most subjects than after small meals. Doubling a small test meal may increase the time by 17 per cent, and trebling it may increase it by 38 per cent. Barclay describes at length the nature of the move- ments in the small intestine. He states (p. 166) that »throughout the intestinal tract peristalsis can be regarded not as the main factor but one of the main reserve mechanismus». He calls attention to the importance of the muscularis mucosae in the transport of food in the small intestine, and suggests that negative pressure may also play a part. In the terminal ileum waves of peristalsis are seen comparatively seldom, and the picture there is a very different one from the restlessness of the duo- denum and jejunum. According to Barclaa' the first of the food is seen in the cae- cum 11 2 2 hours p.c. Baa’liss and Starling (ref. Evans, 3p. 856) describe peris- talsis as a wave moving slowly generally at about 2 cm. a minute involving contraction of the gut above the food mass, and relaxation below it. According to Alvarez (ref. Evans, 3 p. 857), the peristaltic wave as described by Bayliss and Starling, is abnormal, and in his opinion true peristalsis consists of a series of »rushes» traversing the whole length of the small intestine, travelling much more rapidly, 2 to 25 cm. per second. Evans (1.c.) considers that probably both forms of peristalsis occur. Magnusson and Soveri (ref. Lönnerblad, 6 p. 12) found that air can pass through the small intestine in about 10 minutes. Lönnerblad (6. p. 45), using the x-ray method, has examined the transit time of contrast gruel through the small intestine in 109 adults. The volume of the meal was 200 ml. The transit time was reckoned from the time when the test subject had drunk the contrast meal to the moment when the contrast gruel reached the caecum. In none of the test sub- jects was the transit timeless than 30 minutes, and in only 5 cases was it less than 60 minutes. In the majority of cases it was over 2 hours, and in some cases over 5 hours. In their slaughter tests, Ellenberger and Hofmeister (2, p. 295—296) noticed that in swine the emptying of the stomach started during the first hour p.c. when potatoes were fed. 2 hours p.c. 1/3 of the meal had disappeared. When oats were fed, the rate of emptying was low’er, The amounts of food given are not mentioned. E\ans refers to the Amer. J. Physiol. 1938, 123, 44, but we have not been able to find there th quotation in question. SOME OBSERVATIONS ON THE TRANSPORT OF FOOD 3 Out of 500 g. of minced meat 23 % disappeared from the stomach during the first hour p.c., 32 % in the course of 3 hours, 50 % in 5 hours, and 88 % in 12 hours. Neimeier (8 p. 42—45), in his x-ray experiments, fed swine with 400—500 g. porridge which contained ein handvoll von Kartoffelflocken. During the first % hours the emptying of the stomach was especially vigorous. Even while the feeding was going on, the porridge reached the jejunum. Neimeier calls attention to the rush movements in the small intestine. 6—lo hours p.c. the jejunum was empty. The filling of the colon began 2 y 2—3 hours p.c. Hagemeier (ref. Neimeier, p. 15) observed that in the duodenum of the goat the transport of food reaches a velocity of 25—30 cm. in 3 seconds. In Paloheimo’s (1.c.) experiments, the rats, after 12 hours’ fasting, received cakes which were baked from 3g. wheat flour and contained Cr203 as tracer. After this the animals ate dried rye bread ad libitum. The latter circumstance, as Palo- heimo shows, had a delaying effect, especially on the transport of the last remnants of the test meal proper from the stomach to the duodenum. The rats were killed 1,2, 4,6or 9 hours p.c. The amount of tracer still left in the ventriculum is seen in the table below. Hours p.c. when % tracer still eft in rat killed stomach 1 82,3 1 76,5 2 54,6 2 57,4 4 11,9 4 21,3 6 26,1 9 15,9 9 traces 1 hour p.c. the caecum contained traces of Cr2 03 , and 6 hours p.c. only traces of this marker were left in the small intestine. When in the test cakes there was a 50 % substitution of egg white powder, the transport of the marked food was clearly delayed not only in the stomach but also in the small intestine. Goodman et al. (4. p. 236—241) injected 0,5 ml. of an aqueous solution of Evans Blue dye with a soft rubber catheter into the empty stomach of rats, after which the animals were allowed food ad libitum. After 1 hour 50—74 % of the dye was found in the stomach but none in the caecum. After 2 hours 6—30 % was found in the caecum. Stickney et al (13, p. 400—401) studied the rate of passage of an inert test meal in the small intestine of rats weighing between 152 and 370 g. They found that the proportion traversed in 40 minutes was about 72,5 % of the length of the small intestine, independent of the length of the intestine. 4 LAURI PALOHEIMO, AARNE MÄKELÄ AND MAIJA-LIISA SALO Rate of emptying of the rat stomach In the present investigation 33 rats were used. 19 of them were females and 14 males. The age of the females was about 6—7 months, and of the males about 4 months. Notwithstanding the inferiority in age the males slightly exceeded the females in average weight, which was about 200 g. In the behaviour of the two sexes there was no difference discernible in our experiments. The rats were yellow hoods of local breed. For the experiments wheat bread was baked. The dough also contained milk sugar, coco fat, yeast and common salt. The bread was fed dried. The rats were kept without food for 18 hours before being given the experimen- tal meal. They were allowed to eat different amounts of the experimental food and were killed 2 (17 rats) or 3 (16 rats) hours after the beginning of the meal. The amounts of dry matter eaten and of dry matter in the ventriculum were established. They are shown in table 1. Table 1. Dry matter In stomach, Grams of dry matter emptied -2 eaten average from stomach, average during 0 n Z 'o jj? after after first 3rd3 n '3 fr*2 c .5 > 2 hours 3 hours 2 hours houro § ~ 5 g- g- g- g- g- g- -1 8 + 7 2.61—2.87 2.78 0.96 + 0.08 0.31 ±0.07 1.82 0.65±0.11 II 4 + 6 5.39—6.26 5.88 3.52+0.15 2.59+0.15 2.36 0.93+0.21 111 5 + 3 6.62—8.26 7.43 5.00+0.33 4.32+0.50 2.43 0.68 +0.60 The average duration of the meal time in groups I, II and 111 was 14, 28, and 39 minutes respectively. As it is obvious that the emptying of the stomach began before the meal ended, the differences in the charge of the stomach cannot be as sharp as the differences in the amount of dry matter eaten. However, the amounts of dry matter emptied from the stomach during the first 2 hours seem to increase as the amount of the dry matter eaten increases (table 1). In fig. 1 we have plotted the amounts of dry matter transferred from the stomach during the first 2 hours against the amounts of dry matter eaten. The regression is compatible with the equation y = 0.12x+1.52. The following figures show that the animals which were killed 3 hours after the beginning of the meal ate on the average nearly the same amounts of dry matter as their group mates which were killed 1 hour later: 2 hours 3 hours Group I 2.79 g. 2.76 g. » II 5.77 g. 5.96 g. » 111 7.41 g. 7.46 g. SOME OBSERVATIONS ON THE TRANSPORT OF FOOD 5 This observation justifies the calculation of the amount of dry matter emptied from the stomach during the 3rd hour by subtracting in each group the average amount of dry matter in the stomach after 3 hours from the amount after 2 hours. The last column of table 1 shows the results of this calculation. If one compares these figures with the charge of the stomach at the beginning of the 3rd hour, one notices that the last of them (0,68) is unexpectedly low. This figure is rather uncertain, however, because only 3 of the animals of group 111 were killed after 3 hours. From the figures in table 1 one can calculate the amounts of dry matter trans- ferred from the stomach during the 3 hours after the beginning of the meal: Group I 2.47 g. » II 3.29 g. » 111 3.11 g. In fig. 2 is seen the amounts of dry matter transferred from the stomach during the first 3 hours plotted against the amount of dry matter eaten. The regression is compatible with the equation y = 0.19x-f 2.01. Of the total dry matter transport during the first 3 hours, only about 25 % occurred during the 3rd hour. The percentages in groups I, II and 111 were 26.5, 27.7, and 21.7 respectively. Transport of food in the empty small intestine of the rat In the first experiments of this series, adult rats were permitted to fast for 17 hours. During the 24 hours before fasting they were fed with rutabagas only. Dried bread baked from whole kernel wheat meal was used as experimental food. The animals were killed 2,5, 10 or 20 minutes after the beginning of the test meal, and the small intestine was examined immediately after. The procedure of killing the rat and taking out the intestine took about 2 minutes. The following figures show the Dry matter eaten, grams Figure 2. Dry matter eaten, grams Figure 1. LAURI PALOHEIMO, AARNE MÄKELÄ AND MAIJA-LIISA SALO6 distances (from the pylorus) at which the kernel membranes were found in the small intestine at different times after the beginning of the meal: rat No. 1 2 minutes 40 cm. » » 2 5 » 60 » » » 3 5 » 60 » » » 4 10 » 70 » » » 5 10 » 80 » » » 6 20 » 70 » As the small intestine in these rats was about 100 cm. long, the above figures can be regarded as approximate percentages of the whole length of the small intestine. In later experiments 24 hours fasting was maintained and the test bread con- tained Cr20 3 as qualitative tracer. This time we also studied the influence of some variations in the test bread: Bread Nr. I was ordinary wheat bread, in Nr. II ex- tracted soy meal was substituted for 10 % of the wheat flour, in Nr. 11l vegetable oil was used in the same proportion. Nr. IV was not bread at all but beaten and baked egg white. These differences in the composition of food, however, seemed to have no Table 2. T ~ , Rat killed X Advance of food inLength of _. , _, , „ minutes after small intestine Diet Rat small No. No. intestine e^! ' ° the meal cm. from % of length ofcm. ö x= pylorus small intestine 7 100 5 65 65 I 8 100 7 60 60 9 107 10 To 65 10 108 15 81 75 11 95 5 50 53 II 12 101 7 71) 69 13 115 10 '.to 78 14 104 15 80 77 15 107 5 64 60 16 113 7 70 62 111 17 113 10 78 69 18 112 15 85 76 19 109 20 62 57 20 112 5 65 58 21 107 7 62 50 IV 22 109 10 78 72 23 106 15 81 76 24 110 20 80 73 SOME OBSERVATIONS ON THE TRANSPORT OF FOOD 7 Table 3. -n , , ~ j Advance of food in smallRat killed x _ . Length of small , ~ intestineRat ö minutes after intestine ,No. meal cm. _ % of length ofx cm. from pylorus ~ .r J small intestine 25 110 15 82 75 26 117 15 80 68 27 107 25 84 79 28 108 25 83 77 29 119 35 85 71 30 113 35 94 83 31 116 45 96 83 32 114 55 98 86 33 114 65 97 85 34 112 60 104 93 35 111 60 99 89 36 105 75 97 92 37 110 75 100 91 38 106 90 106 JOO 39 111 90 111 100 40 106 105 106 100 41 108 105 108 100 42 100 120 100 100 43 109 120 109 100 distinct influence, if any, upon the rate of filling of the small intestine. Table 2 shows the results of these experiments. One sees that the advance of the food is most rapid during the first 5 minutes and after this lessens considerably. It is noteworthy that the terminal ileum was not less filled than the other parts of the small intestine, but instead of the food contained a yellowish slimy liquid. Evidently the food forced down from the stomach forces the slimy liquid of the »empty» small intestine towards the caecum, the iloecaecal valve still being closed. Thus the small intestine becomes filled in about 5 minutes, the advance of food being thereafter obstructed untill transport to the caecum begins. The above results prompted another series of experiments with longer intervals between the beginning of the meal and the killing of the animals. The diet was about the same as diet lin the previous experiments. The results are seen in table 3 Only rats 40, 42, and 43 have any of the experimental food in the caecum. From these last experiments one may conclude that the transport of food through the ileocaecal valve does not commence until about 1 x/2 hours after the beginning of the meal. 5 u m marv and conclusions Several series of experiments were arranged so as to study in the rat 1) the effect of the degree of the charge of the stomach upon its rate of emptying, and 2) the rate of passage of the food in the empty small intestine. It was observed that the fullness of the stomach had a positive influence on its rate of emptying. In the empty small intestine the transport of the food after the commencement of the meal is very rapid during the first 5 minutes. In this time the food is carried a distance from the pylorus comprising 53—65 % of the length of the small intestine. Five minutes later 65— 78 % of the small intestine contains experimental food. However, the terminal ileum does not appear to be less filled than the other parts of the small intestine. It contains a slimy liquid which has been forced from the »empty» small intestine to- wards the caecum. Evidently the ileocaecal valve has remained closed. Only after about 1 y 2 hours does the food reach the distal end of the small intestine. It is obvious that the rapid filling of the duodenum and jejunum immediately after the beginning of the meal cannot be explained by the classical conception of peristalsis described by Bayliss and Starling. It is remarkable that in the rat the transport of food in the empty small intestine seems to occur at about the same relative rate as in man. REFERENCES (1) Barclay, A. E. 1936. The Digestive Tract, A Radiological Study of its Anatomy, Physiology, and Pathology. Cambridge. (2) Ellenberger und Hofmeister, 1890. Die Verdauung von Fleisch bei Schweinen. Archiv für Physiologie. (3) Evans, L. C. 1947. Principles of human physiology. London. (4) Goodman, R. D., Lewis, A. E., Schukc, E. A. and Greenfield, M. A. 1952. Gastrointestinal Transit. The American Journal of Physiology, 169 (1). (5) Krzywanek, Fr. W. 1926. Vergleichende Untersuchungen über die Mechanik der Verdauung. I. Mitteilung. Einleitung. Untersuchungen am Hund. Pflügers Archiv für die gesamte Phy- siologie des Menschen und der Tiere, 215. (6) Lönnerblad, L. 1951. Transit time through the small intestine. Acta Radiologica. Supplementum 88. (7) Magnus, R. 1908. Die stoppende Wirkung des Morphins. Pflügers Archiv für die gesamte Physio- logie, 122. (8) Neimeier, K. 1939. Röntgenologische Beobachtungen am Magen—Darmkanal des Schweines. I naugural—Dissertation. Hannover. (9) Paloheimo, L. 1939. Über die Verwendung des quantitativen Indikatorverfahrens bei Unter- suchung der Nahrungsfortbewegung im Magendarmkanal. Tierernährung 11. (10) Rieder, H. 1925. Die physiologische Dünndarm Bewegung beim Menschen. Fortschritte auf dem Gebiete der Röntgenstrahlen, 33. (11) Scheunert, A. und Trautmann, A. 1951. Lehrbuch der Veterinär-Physiologie. Berlin. (12) Schinz, H. R., Baensch, W. E., Friede, E., Uehlinger, E. 1952.Lehrbuch der Röntgendiagnostik. 7. Lieferung. Stuttgart. (13) Stickney, J. C., van Liere, E. J., and Northup, D. W. 1951. Correlation Between Propulsive Motility and Length of the Small Intestine in Albino Rats and Dogs. The American Jour- nal of Physiology, 167 (2). (14) Swiney, B. A. and Spurrell, W. R. 1935. The Effect of Fat on Gastric Motility. The Journal of Physiology, 84. LAURI PALOHEIMO, AARNE MÄKELÄ AND MAIJA-LIISA SALO SOME OBSERVATIONS ON THE TRANSPORT OF FOOD 9 SELOSTUS: ERÄITÄ HAVAINTOJA RUOAN KULUSTA ROTAN RUOANSULATUSKANAVASSA Lauri Paloheimo, Aarne Mäkelä ja Maija-Liisa Salo Kotieläintieteellinen laitos, Helsingin Yliopisto Kirjoittajat ovat etsineet selvitystä seuraavaan kahteen kysymykseen: 1) mahalaukun kuormitus- asteen vaikutus sen tyhjentymisnopeuteen ja 2) ravinnon kulkunopeus tyhjässä ohutsuolessa. Edellisen kysymyksen tutkimiseen käytettiin 33 ja jälkimmäisen 43 rottaa. Todettiin, että mahalaukun täytei- syydellä oli positiivinen vaikutus sen tyhjenemisnopeuteen. Ruoansulatuskanavan ollessa tyhjän umpi- suolta myöten, siirtyy osa mahalaukkuun tulleesta ruoasta välittömästi ohutsuoleen jaetenee siellä tavat- toman nopeasti. Viidessä minuuttissa aterian alkamisesta laskien etenee ruoka 53—65 % ohutsuolen pituudesta. Kuitenkin kestää n. 1 % tuntia ennenkuin ruoka ehtii ohutsuolen loppupäähän. Osoittau- tui, että ruoan edettyä n. 75 % ohutsuolen pituudesta myös ohutsuolen loppupää oli täysinäinen, sisäl- täen ruoan edellä sinne työntynyttä limaista nestettä, joka umpisuoleen johtavan aukon pysyessä sul- jettuna ei vielä voinut tulla tyhjennetyksi umpisuoleen. BAYLissin ja SxARLiNGin klassillinen käsitys suolen peristaltiikasta ei riitä selittämään näissä kokeissa todettua ruoan nopeata etenemistä tyhjässä ohutsuolessa.