EPITHELIAL CELL KINETICS IN THE SMALL INTESTINE OF THE RAT 60 DAYS AFTER RESECTION OF 70 PER CENT OF THE ILEUM AND JEJUNUM
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1 GASTROENTEROLOGY Copyright 1971 by The Williams & Wilkins Co. Vol. 60, No.6 Printed in U. S. A. EPITHELIAL CELL KINETICS IN THE SMALL INTESTINE OF THE RAT 60 DAYS AFTER RESECTION OF 70 PER CENT OF THE ILEUM AND JEJUNUM WAYNE R. HANSON, AND JAMES W. OSBORNE, PH.D. Radiation Research Laboratory, College of Medicine, University of Iowa, Iowa City, Iowa Sixty days following resection of 7 0 ~ of c the small intestine, excluding duodenum, several parameters of the remaining crypt cell population were measured by means of autoradiography using tritiated thymidine as a nuclear label. The S phase was the portion of the cell cycle most affected and was reduced an average of 9 ~ in ~ all intestinal segments from resected animals. The generation time decreased slightly owing to shortening of the S phase. The increased length and cellularity of crypts indicated hyperplasia. The total proliferative population increased proportionally with the increase in crypt size, both increasing about 36.5% which resulted in no change in the labeling index. The mitotic index increased an average of 22% but this represents an average from 3.7)c in sham-resected to 4.5% in resected animals. The migration rate of epithelial cells from crypts to villi was increased an average of 31 %. Experimental resection of intestine, mainly in dogs and rats, has been carried out by a number of investigators.1-12 Most of these have been concerned with morphological,1-4, 9, 11 physiological, 1, 3, 1, 10, 12 and biochemical 5, 6, 8 changes noted after the removal of various lengths of small intestine. Reports of gross changes in morphology and physiology following resection of human intestine necessitated by pathological conditions such as volvulus, stran- Received July 6, Accepted January 22, Address requests for reprints to: Dr. James W. Osborne, Radiation Research Laboratory, University oflowa, Iowa City, Iowa Wayne R. Hanson was the recipient of a National Defense Education Act IV Fellowship during a portion of the period devoted to this research. The supply grant, awarded with the Fellowship, and Public Health Service Research Grant AM-11206, National Institute of Arthritis and Metabolic Diseases, provided partial support for this study. This study was conducted in partial fulfillment of the requirements for a Master of Science degree in Radiation Biology at the University of Iowa. The authors wish to thank Mrs. John Brandt and Mr. James Raney for superb technical assistance gulated hernia, and mesenteric thrombosis were reviewed by Pullan 13 and Jackson. 14 The suitability of tritiated thymidine ehtdr) as a nuclear label has given much impetus to the study of cell population kinetics in the residual intestine following resection. Loran and co-workers I5-11 have used 3HTdR and autoradiography to study various parameters of the cell kinetics of intestinal epithelial cells in the rat 2 months after resection of an ileal segment equivalent to 10% of the small intestine. They found that increases in cell renewal rate and height of villi occurred in the intestine which remained after a resection. The paper of Knudtson et al. 18 disagreed with the results of Loran and co-workers. After a resection of 50)0 of the proximal small intestine in the rat and the subsequent injection of 3HTdR, they found no differences in numbers of labeled nuclei or in specific activity of tritium-labeled deoxyribonucleic acid (DNA) among control, transected, or resected animals. Skala et al., 19 using planimetric methods, found that, 3 weeks after a 50% resection
2 1088 HANSON AND OSBORNE Vol. 60, No. 6 of the small intestine, the absorptive surface roughly doubled and thereby nearly equaled the original area. They felt that the increase resulted from mucosal hypertrophy and elongation of the villi. Sigdestad and Osbome 20 assessed the effect of resecting 70 )0 of the combined ileum and jejunum on the survival time of rats given X-irradiation to the remaining ileum and jejunum. They found that a 70% resection afforded protection which was enhanced with increased time between surgery and irradiation and was decreased with increased X-ray exposure. The maximum time interval tested between surgery and irradiation was 60 days, at which time the greatest protective effect was seen. However, determination of the cellular status of the residual intestine was not undertaken in those experiments. One purpose of this investigation was to measure some of the cell population kinetic parameters of the residual small intestine 60 days after resection of 70% of the combined ileum and jejunum and to determine whether a resection, approaching the maximum compatible with survival, leads to responses substantially different from those reported by Loran and co-workers.i5. 16 Additionally, the results will be of value in determining whether the increased radioresistance of the residual ileum and jejunum could have its basis in cell renewal changes. Materials and Methods Surgical techniques. Male Holtzman rats weighing 250 to 300 g were fasted for 12 hr prior to surgery and anesthetized with an intraperitoneal injection of pentobarbital sodium, 40 mg per kg of body weight. A midline laparotomy was performed and the intestine from the ligament of Treitz to the cecum was exteriorized. The 70% resection was done as previously described! Sham resection consisted of exteriorization of the small intestine for the same length of time that it took to perform a resection (about 30 min). The gut was returned to the peritoneal cavity and the wound was closed as before. Animals and animal care. As previously reported by Sigdestad and Osborne,2. there was a small initial weight loss during the postoperative period of rats subjected to gross resections of the small intestine. This loss was followed by a normal growth pattern which paralleled and was close to control animals. At the end of 60 days, the weight and general health of all animals tested in this experiment were similar and good, respectively. Groups of 5 resected and 5 sham-resected animals were caged together in wire bottom cages in one room at constant temperature with a 12-hr light-dark cycle. For the first 24 hr postoperative, the animals were given 5% sucrose. On the 2nd day, 5% sucrose and a small amount of laboratory chow in pellet form were allowed. Rat chow and tap water ad libitum were allowed beginning the 3rd postoperative day. Tissue preparation and autoradiography. Sixty days after their operation, 34 resected animals and 34 sham-resected animals were injected with 3HTdR, specific activity 6.0 c per mmole, 50 p'c per 100 g of body weight. Two resected and 2 sham-resected animals were killed with ether at the following times after injection: V2 hr, 1 hr, 2 hr, 3 hr, 5 hr, 7 hr, 8 hr, 9 hr, 10 hr, 11 hr, 12 hr, 13 hr, 14 hr, 15 hr, 17 hr, 18 hr, and 19 hr. Intestinal segments were taken from three sites: (1) 1 cm distal to the ligament of Treitz, (2) the site of resection in resected animals or from the center of the intestine in sham-resected animals, and (3) 1 cm proximal to the ileocecal junction. The pieces of intestine were cut open, stapled to a piece of cardboard, and fixed in 10 )0 formol-saline. Tissues were embedded in paraffin, and autoradiographs were prepared by dipping slides containing 3p.-unstained tissue sections in Eastman Kodak NTB emulsion and storing them in a lighttight box at 4 C for 8 days. The slides were developed in Eastman Kodak D-ll developer, fixed in hypo, rinsed in tap water, and stained with Harris hematoxylin. Sections prepared by this method presented only occasional background grains but approximately 20 grains for labeled nuclei when viewed under oil immersion (X 1000). All cell counts were made using oil immersion and, since a range of grains per labeled nucleus existed, an arbitrary cutoff point of six grains was used; i.e., if a cell had six grains or more over its nucleus, it was counted as being labeled. The number of grains over labeled nuclei was sufficiently high as to cause very few borderline cases. Cell cycle time and length of various components. For each segment of every animal, 100 mitoses in metaphase and anaphase stages were scored for label and the percentage of labeled mitoses was calculated. The percentage of labeled mitoses was plotted as a function of time after injection of 3HTdR; the method of Lesher et al. 21 was used to calculate the duration of the
3 June 1971 EPITHELIAL CELL KINETICS 1089 total cell cycle time (GT) and the length of each phase, i.e., G 1, S, G 2, and M. Crypt cell count technique for determination of labeling index and mitotic index. Ten resected and 10-sham-resected animals were injected with 3HTdR, 6.0 c per mmole, 50 JLC per 100 g of body weight, and killed 1 hr later. The intestinal segments of interest were fixed and sectioned and autoradiographs were prepared. Sections showing the base, lumen and top of six crypts were selected and the following parameters were estimated: (1) total cells per crypt section, (2) labeled cells per crypt section, and (3) number of mitoses per crypt section. The labeling index, defined as the number of labeled nuclei in the crypt section per total number of nuclei in the crypt section, was calculated. The mitotic index, defined as the number of metaphase and anaphase mitotic figures per crypt section per total number of cells in the crypt section, was also determined. Comparisons between the different segments of intestine in terms of the number of cells per crypt section and the number of labeled cells per crypt section were also made. Migration rates. Additional tissue sections were used to determine the migration rate of cells from the lower two-thirds of the crypt to the villus. Only sections in which the gross lumen of the intestine was continuous with the lumen of crypts were used. The position occupied by the labeled cell which had moved the farthest from the center of the bottom of crypts 1, 9, and 17 hr after the injection of 3HTdR was determined in a manner described by Cairnie et al. 22 The migration rate was then calculated by dividing the number of cell positions moved by the time interval between measurements. Statistical treatment of data. The portion of the experiment to determine labeled cells per crypt section, total cells per crypt section, mitotic index, and labeling index was designed as a completely random 2 X 3 factorial. An analysis of variance was used to test for significant differences resulting from: (1) resection, (2) site sampled, and (3) interaction of site and type of resection. Statistical limits (95% confidence intervals) were determined for the treatment group by means of cell positions of the topmost labeled epithelial cells as measured from an established reference point in the center of the bottom of the crypts. Results At the time of killing, no gross morphological changes in the intestine of sham-resected rats were seen. However, in resected rats, the circumference of the intestine was greater at the site of the end-to-end anastomosis. This increase appeared equal on both sides of the anastomosis and tapered off slowly proximally and distally. When the intestine of resected rats was cut lengthwise and flattened prior to fixation, an elevation of mucosa at the suture line was apparent, but not pronounced; it was clear that there had been no intestinal obstruction. When observed microscopically, the mucosa was continuous over the thickened tissue at the site of resection (fig. 1). Generation time and cell cycle components. The mean percentage of labeled mitoses in all segments of individual animals for both resected and sham-resected animals was calculated and plots of percentage of labeled mitoses versus time for each of three sites sampled in resected and sham-resected animals were made. There was little difference among sites within each treatment group, particularly in the first ascending and descending limbs of the curves. However, in comparing the percentage of labeled mitoses curves for each site in the resected animals with its comparable site in the sham-resected animals, the first descending limb of the curve for resected animals always preceded the first descending limb of the curve for sham-resected animals (figs. 2 to 4). In sites 1 cm distal to the ligament of Treitz (upper jejunum) and midway between the ligament of Treitz and the cecum (median small intestine), the second ascending limb of the curve for resected animals likewise preceded the one based on data from sham-resected animals. The generation times and the lengths of cell cycle phases are given in table l. The S phase in all segments of small intestine from resected animals was reduced when compared with analogous segments in shamresected animals. The generation time in segments of the upper jejunum and median small intestine was shorter in resected animals than in sham-resected animals. In segments 1 cm proximal to the cecum (lower ileum), the generation time was longer than in sham-resected animals; in this case, G 1 was longer in the resected animals than in the sham-resected animals. Number of cells per crypt section, number
4 1090 HANSON AND OSBORNE Vol. 60, No.6 FIG. 1. Low power photomicrograph showing the anatomical change in the intestine resulting from an end-toend anastomosis (X 100). of labeled cells per crypt section, labeling index, and mitotic index. The mean number of cells per crypt section in all sites of intestine sampled was significantly greater in resected animals than in sham-resected animals (figs. 5 to 7). There was no significant difference among sites within either resected or sham-resected 'animals (table 2). Thus resection caused an increase in the crypt population throughout the residual intestine. ill resected rats there was an increase in the number of labeled cells per crypt section compared with sham-resected rats (figs. 5 to 7). This increase occurred in all three sites (table 2). The labeling index was unchanged in the resected intestine compared with the sham-resected intestine irrespective of site. The mitotic index was increased in all sites of resected compared with sham-resected animals. Migration rates. The locations of the top labeled epithelial cells expressed as the number of cell positions from the center of
5 June 1971 EPITHELIAL CELL KINETICS 1091 RESECTED " 80 w." o 70 ~ i 60 o 50 w ~ 40 al ~ 30 ~ SHAM - RESECTED 0 L - ~ ~ 2 ~ ± 3 ~ 4 ~ ~ 5 ~ = - ~ 8 ~ 9 ~ ~ 1 0 ~ 1 ~ 1-1 ~ 2 ~ 1 ~ 3 ~ HOURS AFTER INJECTION OF 3HTdR FIG. 2. Percentage of labeled mitotic figures (metaphase and anaphase) versus time after injection of 'HTdR in segments 1 cm distal to ligament of Treitz from resected and sham-resected animals. Each point represents the mean percentage of labeled mitoses from 2 animals. One hundred mitotic figures were counted from each animal ~ 8 0." 8 70 i60 _... RESECTED - SHAM - RESEC TE D D\ it '0 ~ ~ : \ \ / ~ ) \ at 20 \\ j /. 10 \ X_ 0 L ~ 2 ~ 3 ~ + 4 ~ 5 ~ 6 ~ ~ 7 ~ 8 ~ 9 ~ ~ 1 0 ~ 1 ~ 1 ~ 1 ~ 2 ~ 1 3 ~ 1 ~ 4 HOURS AFTER INJECTION OF 3HTdR FIG. 3. Percentage of labeled mitotic figures (metaphase and anaphase versus time after injection of 'HTdR in segments midway between the ligament of Treitz and cecum from resected and sham-resected animals. Each point represents the m9a1l percentage of labeled mitoses from 2 animals. One hundred mitotic figures were counted from each animal. the bottom of crypts in both resected and sham-resected animals are shown in table 3. The average migration rates in the sites tested are given in table 4. ill the first 10 hr following the injection of 3HTdR, the migration rates of cells in all sites of sham-resected animals were similar (table 4). The cell migration rates during the 10- to 17-hr period were faster than the 1- to 10-hr rates at all sites. However, the rate of cell movement in the lower ileum, during the period 10 to 17 hr after injection of 3HTdR, was slower than the rates in the other two sites. With the exception of the value for the site near the cecum (C, 10 to 17 hr in table
6 1092 HANSON AND OSBORNE Vol. 60, No.6. RESECTED on ~ 80 ~ 70 ~ 60 fil 50 -' ~ 40 < -' 30 ~ - SHAM RESECTED HOURS AFTER INJECTION OF 3HTdR FIG. 4. Percentage of labeled mitotic figures (metaphase and anaphase) versus time after injection of 'HTdR in segments of 1 cm proximal to cecum from resected and sham-resected animals. Each point represents the mean percentage of labeled mitoses from 2 animals. One hundred mitotic figures were counted from each ani mal. TABLE l. Durations of the generation time (e7) and the separate components G,. S. G 2, and M in resected and sham-resected rats" G, S G, M GT Resected rats 1 cm distal to ligament of Treitz Midway between ligament of Treitz and cecum em proximal to cecum Sham-resected rats 1 cm distal to ligament of Treitz Midway between ligament of Treitz and cecum em proximal to cecum a Values in hours calculated from formulas used by Lesher et al. 21 4), the migration rates for cells in resected animals were always higher than the rates for analogous periods in sham-resected rats. Discussion The intestinal enlargement observed after resection was similar to that noted in other reports , 23 In two papers, an increased diameter in the postanastomotic intestine only3 or increases both proximally and distally with the greatest increase distal to the resection site were found,23 but resection of 50% or more of the small intestine was involved whereas lesser resections were used in most of the investigations cited earlier. Some intestinal enlargement in resected animals of the present study was noted both distally and proximally, but no measurements were taken. The S phase was the portion of the cell cycle most affected by resection and was reduced in all segments of resected animals as compared with control animals. The reduction was slight in the lower ileum and may not represent a significant difference. The shortened S phase was the major factor causing the slightly reduced generation time in the upper jejunum and median small intestine. The major contributing factor to the discrepancy between the lower ileum and the other two sites was an increased G 1 phase. Estimation of a long G 1 phase resulted from a dip in the second ascending curve in the lower ileum and may not represent an accurate G I value. Over-all, the findings are similar to those of Lora!1. and Crocker. IS There was no increase in the labeling index at any site tested. Although the number of labeled cells per crypt section was increased following resection, so was the total
7 June 1971 EPITHELIAL CELL KINETICS 1093 FIG. 5. Photomicrographs of longitudinal section through crypts 1 cm distal to ligament of Treitz in resected and sham-resected rats. Both photomicrographs were taken at same power (X 5(0). Tissues were fixed 1 hr after injection of 'HTdR. number of cells per crypt section. Thus a 70S~ resection caused increases in both the total cell population and the proliferative compartment of each crypt if it is assumed that increased cells per longitudinal crypt section indicate an increased total population. This represents a significant deviation from the results of Loran and Crocker, 16 who reported a large increase in the percentage of labeled cells per crypt section at 1/ 2 hr after injection of 3HTdR but no increase in the total crypt population. The difference in their results compared with those of the present report may be only the result of the vast difference in the amount of intestine removed, since there were only minor differences in other procedures. Knudtson et al. 18 claimed that there was no difference in response among resected, transected, and control rat small intestine when the end points of labeled nuclei found in eight high power fields and changes in specific activity of tritium-labeled DNA were used. Although the use of "fields" might offer certain advantages, the usefulness in estimating the size of the prolifer-
8 1094 HANSON AND OSBORNE Vol. 60, No.6 FIG. 6. Photomicrographs of longitudinal sections through crypts midway from the ligament of Treitz to cecum in resected and sham-resected rats. Both photomicrographs were taken at the same power (X 500). Tissues were fixed 1 hr after injection of 3HTdR. ative compartment is limited. A lack of change in the specific activity of tritiumlabeled DNA does not rule out a change in size of the proliferative compartment since a change in activity per DNA weight could only be obtained if the shift in the proliferative compartment size was not proportional to the change in mucosal cellularity. With 70% resection, the mitotic index in intestines from resected animals was slightly but significantly increased, which at first seemed contradictory as there was no increase in the labeling index. However, the small increased mitotic index could be the result of a decrease in total generation time. The average migration rates of labeled epithelial cells from 1 to 17 hr after the injection of 3HTdR were faster in resected than in sham-resected animals. The fastest rate was at the site of anastomosis and agrees with the results of Loran and coworkers. 15, 16 The effect on the migration rate in the lower ileum was minimal and, in fact, the migration rate of the leading edge from 10 to 17 hr after injection of 3HTdR was less in resected rats than in sham-re-
9 June 1971 EPITHELIAL CELL KINETICS 1095 FIG. 7. Photomicrographs of longitudinal section through crypts 1 cm proximal to cecum in resected and sham-resected animals. Both photomicrographs were taken at the same power (X 500). Tissues were fixed 1 hr after injection of 'HTdR. sected rats. The migration rates of epithelial cells from crypts to villi were not steady, as shown by the slower rate of cell movement from 1 to 10 hr compared with 10 to 17 hr after injection of label. The 4-hr delay between the onset of differentiation and migration as observed by Quastler and Sherman24 is a plausible explanation for the slower rate of migration during the 1- to 10-hr interval. The migration rate in the crypts of resected animals was also less than the rate of movement on the villi. Thus, there may be a similar delay in the crypts of resected animals but not as great a delay as in sham-resected animals. The effect of a delay, if present in resected animals, was less at the resection site than on either side of it. The cellular status of the residual small intestine 60 days after a 70% resection was as follows: (1) the total generation time decreased slightly owing to a decrease in the S phase; (2) hyperplasia existed in the crypts as shown by increased length and cellularity; (3) the total proliferative population increased proportionally with the increase in crypt size; (4) the mitotic index increased slightly; and (5) the average migration rates
10 1096 HANSON AND OSBORNE Vol. 60, No.6 TABLE 2. Number of cells per crypt section, number of labeled cells per crypt section, labeling index (percentage) and mitotic index (percentage) in resected and sham-resected animals Site No. of animals Number of Number of Treatment cells per crypt labeled cells Labeling index Mitotic index, section per crypt section,, Aa 10 Resected 82.6\-, 24.4" ~ b NS / / 4.\ 10 Sham -resected rI / Be 10 Resected ~ 2 8. ~ ~ S ys / /S 10 Sham -resected (/ Cd 10 Resected , 86.> 4.4" S 28.?S? 10 Sham -resected ! 3.6 a A, 1 cm distal to ligament of Treltz. b Separate analyses of variance for significance (S) or nonsignificance (NS) were calculated for each category of means using the P = 0.05 level. The analyses of variance were designed to test the difference within treatment groups, between treatment groups, and interaction between site and treatment groups. In no case was there any significant difference within a treatment nor was there any significant interaction. c B, midway between ligament of Treitz and cecum. dc, 1 cm proximal to cecum. TABLE 3. Locations of topmost labeled epithelial cells expressed as the number of cell positions from the center of the bottom of crypts a Hours after Resected Sham -resected injection of 'HTdR A" B' C" A B C ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1.5 a Each value represents the mean with a 9 5 confidence ~ c interval based on the cell positions determined from a minimum of 35 crypt halves from 2 animals. b A, 1 cm distal to ligament of Treitz. c B, midway from ligament of Treitz to cecum. dc, 1 cm proximal to cecum. of epithelial cells from crypts to villi were increased. The results can be used to propose a plausible mechanism to explain the decreased radiosensitivity of intestine-irradiated rats as reported by Sigdestad and Osborne. 20 Survival of an animal after exposure of the intestine to an amount of X-radiation sufficient to denudate the mucosa depends on several things, among them the ability of the surviving epithelial cells to regenerate a normal mucosa. This ability is, in tum, related to the number of cells present in the crypt after irradiation which are still capable of proliferation. Considering the individual unit of the crypt as a regenerative focus following radiation damage, the ability of the crypt to regenerate the crypt to villus relationship would depend on the size of the proliferative compartment in each crypt and not on the total number of proliferative cells in the intestine. The results of this experiment have shown that, 60 days following resection, a larger proliferative compartment in each crypt exists, thereby creating a hyperplastic mucosa. It is then likely that this is at least one of the mechanisms involved in increasing the survival time of intestine-irradiated rats which have previously undergone intestinal resection.
11 June 1971 EPITHELIAL CELL KINETICS 1097 TABLE 4. Average migration rates of epithelial cells at three sites of resected and sham-resected intestines a Period of Resected Sham-resected t.ime after injection of ' HTdR A' B' C' A B C hr a Values given are average cell positions moved per hr calculated by dividing the difference between cell positions at various times after injection of 'HTdR by the hours elapsed at time of measurement (table 3). No statistical limits are given as this would imply that the migration rate is steady from crypt to villus. A, 1 cm distal to ligament of Treitz. C B, midway from ligament of Treitz to cecum. dc, 1 cm proximal to cecum. REFERENCES 1. Bochkov NP: Morphological and physiological changes in the small intestine of the dog after its partial resection. Bull Exp Bioi Med 46: , Bochkov NP: Morphological changes in the jejunum and ileum of rats after wide resection of the small intestine. Bull Exp Bioi Med 47: , Dowling RH, Booth CC: Structural and functional changes following small intestinal resection in the rat. Clin Sci 32: , Flint JM: The effect of extensive resections of the small intestine. Bull Johns Hopkins Hasp 23: , Jesseph HE, Jacklin AJ: Effects of partial resection of mammalian small intestine. III. Glucose absorption, CO, production and blood flow in residual ileum in the dog. Rev Surg (Phila) 20: , Loran MR, Althausen TL: Transport of vitamin A in vitro across normal isolated rat intestine and intestine subjected to "partial" resection. Amer J Physiol 197: , Nygaard K: Resection of the small intestine in rats. I. Nutritional status and adaptation of fat and protein absorption. Acta Chir Scand 132: , Nygaard K: Resection of the small intestine in rats. II. Absorption of vitamin B 1 " with special regard to adaptation of absorption. Acta Chir Scand 132: , Nygaard K: Resection of the small intestine in rats. III. Morphological changes in the intestinal tract. Acta Chir Scand 133: , Nygaard K: Resection of the small intestine in rats. IV. Adaptation of gastro-intestinal motility. Acta Chir Scand 133: , Nylander G, Olerud S: Intestinal adaptation following extensive resection in the rat. Acta Chir Scand 123:51-56, Loran MR, Althausen TL, Irvine E: Effects of "minimal" resection of the small intestine on the absorption of vitamin A in the rat. Gastroenterology 31: , Pullan JM: Massive intestinal resection. Proc Roy Soc Med 52:31-37, Jackson WPU: Massive resection of the small intestine, Modern Trends in Gastro-enterology, 2nd series. Edited by FA Jones. New York, Paul B Hoeber Inc, 1958, p Loran MR, Althausen TL: Cellular proliferation of intestinal epithelia in the rat two months after partial resection of the ileum. J Biophys Biochem Cytol 7: , Loran MR, Crocker 11: Population dynamics of intestinal epithelia in the rat two months after partial resection of the ileum. J Cell Bioi 19: , Loran MR, Carbone JV: The humoral effect of intestinal resection on cellular proliferation and maturation in parabiotic rats, Gastrointestinal Radiation Injury. Edited by MF Sullivan. Amsterdam, Excerpta Medica Foundation, 1968, p Knudtson KP, Priest RE, Sloop RD, et al: Effects of partial resection of the mammalian small intestine. II. Cell renewal of intestinal epithelium in the rat, with special reference to the colon. Lab Invest 12: , Skala I, Hromadkova V, Skala J: Hypertrophy of the small intestine after its partial resection in the rat-size of the mucosal surface. Digestion 2: 23-34, Sigdestad CP, Osborne JW: The influence of prior intestinal resection on survival time of intestineirradiated rats. Int J Radiat Bioi 15:65-73, Lesher S, Lamerton LF, Sacher GA, et al: Effect of continuous gamma irradiation on the generation cycle of the duodenal crypt cells of the mouse and rat. Radiat Res 29:57-70, Cairnie AB, Lamerton LF, Steel GG: Cell proliferation studies in the intestinal epithelium of the rat. I. Determination of the kinetic parameters. Exp Cell Res 39: , Knudtson KP, Priest RE, Jacklin AJ, et al: Effects of partial resection on mammalian small intestine. I. Initial autoradiographic studies in the dog. Lab Invest 11: , Quastler H, Sherman FG: Cell population kinetics in the intestinal epithelium of the mouse. Exp Cell Res 17: , 1959
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