The surface pattern of the and in a chronic renal failure cohort

JOHN H. SCOTT, DD. Pottsville, Pennsylvania ROBERT R. ROSENBAUM, aa, FAOCR Philadelphia, Pennsylvania

nostic imaging studies did not confirm the presence A retrospective review of 42 patients of malignant disease, and renal transplantation (60 examinations) with end-stage was successfully performed. This experience renal disease (ESRD) on dialysis prompted a review of the literature dealing with therapy was performed for evaluation the appearance of the upper of the roentgenographic appearance in end-stage renal disease (ESRD) patients on di- of the upper gastrointestinal tract. alysis as well as a retrospective review of our mate- Many patients with chronic renal rial. The purpose of this report is to document our failure exhibited a variation in the findings. surface pattern of the stomach and Method duodenum during maintenance dialysis therapy. There was an Sixty upper gastrointestinal tract examinations, increased incidence of a cobblestone which had been performed for 42 ESRD patients configuration of the duodenal who were on maintenance dialysis between 1979 mucosa, predominantly within the and 1983, were evaluated retrospectively for the duodenal cap and proximal duodenal purpose of analyzing the following parameters: (1) loop. These nodular defects are quality of gastric surface pattern visualization; (2) probably representative of thickness of and presence or absence of nodular hypertrophy of Brunners glands and defects of the gastric mucosal folds; (3) presence, should not be mistaken for possible number, and size of nodular surface pattern defects malignant submucosal lesions. In the in the cap and duodenal loop; and (4) presence of patients who presented with similar gastric or cap ulcers. complaints of , Of the 60 studies, 45 were performed by a stan- there was only a small incidence of dard double-contrast method. 1 The remainder were peptic ulcer in the ESRD cohort as single-contrast examinations, usually because of compared to the group without renal the inability of the patient to cooperate sufficiently failure. Because of the increase in for an adequate double-contrast procedure. incidence of maintenance dialysis A random control study was then performed therapy in ESRD patients, we suggest retrospectively in patients of similar age (40-65 that these findings are of importance years) who presented with complaints of peptic ul- in a radiographic assessment of the cer disease. Sixty patients were examined between upper gastrointestinal tract. September and December 1983; all 60 underwent double-contrast upper gastrointestinal examina- tions. The same parameters were utilized in the evaluation of these studies.

Review of the literature References to the appearance of the upper gastroin- A patient who had been on a hemodialysis regimen testinal tract in ESRD (particularly as demon- for chronic renal failure was subjected to radiologic strated by double-contrast techniques) are sparse. assessment of the upper gastrointestinal tract in This is somewhat surprising in view of the increas- anticipation of a renal transplant procedure. The ing number of such patients. There is a large body study demonstrated multiple large nodular surface of literature dealing with the gross and microscopic pattern defects in the duodenal loop, which were pathology of the mucosa, endoscopic appearance of interpreted as possible malignant submucosal the mucosa, and physiologic parameters of acid masses (Fig. 1). Endoscopic and other diag- production, secretory activity, and so forth, with

Surface pattern of the stomach and duodenum in a chronic renal failure cohort 162/75 thickened mucosal folds without nodules. Endo- scopic evaluation correlated directly with the radi- ographic findings of nodular duodenitis. Histologic characteristics of nodular duodenitis suggested this to be a form of duodenal . Of interest is the incidence of peptic ulcer disease in only 6 percent of these patients versus the overall incidence of peptic ulcer disease in 1-3 percent of the general population. 12 Zuckerman and col- leagues concluded that nodular duodenitis may be a variation in the clinical presentation of peptic ulcer disease in the patients with ESRD. Weiner, Vertes, and Shapiro° performed upper gastrointestinal tract studies on 48 patients, 14 of whom were on peripheral dialysis and 34 on hemo- dialysis. There were 10 abnormal examinations in Fig. 1 Double-contrast upper gastrointestinal study of a pre- the peritoneal dialysis group and 23 in the hemo- transplant patient with chronic renal failure demonstrates nodular defects in the duodenal loop ( arrows). dialysis patients. The listed abnormalities in- cluded the following: a "wet stomach" with prominent gastric folds in 11 patients; prominence some passing references to radiologic examina- and enlargement of duodenal bulb folds, usually tion.2-9 linear and irregular but occasionally vertical and/ Lewicki and associates l° reviewed 51 upper gas- or nodular in 21 patients; duodenal ulcer scarring trointestinal studies in a group of 235 patients, in 3 patients; and prominence of mucosal pattern some of whom were on pretransplant dialysis and with enlarged folds involving the proximal portion most of whom were post-transplant patients. Gas- of the descending duodenum in 8 patients. There trointestinal bleeding was the most common in- were no gastric or duodenal ulcers. dication for examination. Thirty-three studies King and coauthors" reported on 22 upper gas- were normal, and 15 patients had gastroduodenal trointestinal and small bowel studies in 18 patients ulcerations. A duodenal mucosal pattern resem- on hemodialysis. Fourteen studies had normal bling that associated with Brunners gland hyper- findings. The remaining studies demonstrated trophy was seen in 80 percent of the dialysis mucosal changes of the duodenum, , and patients and 60 percent of the post-transplant pa- , including thickened but pliable valvulae tients. The authors called this a "cobblestone duo- conniventes. There were no gastric abnormalities. denal mucosa" and commented that "widened In a prospective study of 83 renal failure patients rugae and enlarged duodenal mucosal folds were on dialysis, Margolis and coworkers 15 observed en- common. Because of technical factors, it was gener- larged gastric folds in 12 percent and enlarged duo- ally easier to assess and grade this finding in the denal folds in 42 percent. No peptic ulcers were duodenum." In a group of randomly selected ulcer demonstrated. Correlative panendoscopy in 60 of patients without known renal failure, a distinct the 83 patients demonstrated in 22 per- cobblestone pattern was seen in 23 percent. The cent and nodular duodenitis in 60 percent. A highly threefold-increased incidence of such a pattern in significant correlation existed between endoscopic their renal failure groups led to the conclusion that and radiologic duodenitis. it could not be merely a secondary feature of ulcer Smith, Petersen, and Junor 16 demonstrated hy- disease, but that a mechanism related to altered pertrophy of in 19 and hypertrophy renal function was responsible. of the duodenal mucosa in 11 of 31 patients who Zuckerman and colleagues 11 evaluated the duo- were on long-term hemodialysis. Three patients denum in patients with ESRD by radiographic and had questionable ulcer disease radiographically, endoscopic methods. Seventeen of 50 patients (34 but no ulcers were observed endoscopically. percent) had radiographic findings of "nodular duo- Dorph and associates 17 found a coarse mucosal denitis," which was defined as two or more discrete pattern in 65 percent of 84 studies in chronic renal nodules protruding into the duodenal lumen. Four failure patients. The most common location was in percent exhibited these findings in the general pop- the distal half of the duodenal bulb and in the ulation. An additional 15 patients (30 percent) de- proximal half of the descending duodenum. Only 1 picted findings of "non-nodular duodenitis," that is, peptic ulcer was seen.

163/76 March 1986/Journal of AOA/vol. 86/no. 3 Results Gastric surface pattern The double-contrast studies were evaluated for quality of surface pattern demonstration. Cur- rently acceptable criteria for a good surface pattern are based on sharpness of the areae gastricae pat- tern—sharpness and continuity of the "white line" marginal contour of the stomach and the area of the stomach throughout which the pattern is apparent (Fig. 2A). It is generally anticipated that a good surface pattern is obtained in about 50 percent of unselected double-contrast studies. The surface pattern was judged as poor, fair, or good. A surface pattern was judged as poor if no areae gastricae were visualized, or if only a small segment of the stomach contained identifiable areae gastricae, or if extensive puddling of barium occurred (Fig. 2B). A fair designation was given to an areae gastricae pattern that was somewhat more extensive but obviously limited to well under 50 percent of surface area without extensive pud- dling of barium (Fig. 2C). The 45 double-contrast studies presented 31 poor, 10 fair, and 4 good surface pattern (Table 1). In the population without renal failure, there were 46 good and 14 fair surface patterns.

Mucosal folds The appearance of the gastric mucosal folds was evaluated in all 60 examinations, in an effort to assess prominence, nodularity, or other abnor- malities. Prominence of gastric folds is difficult to define. In this review, those cases that appeared to have thicker than average folds or coarser and more irregular than average folds were designated as prominent. Nodular defects were recorded when round, sharply marginated lucent zones, fixed in position, without evidence of pedicles, in the ab- sence of luminal narrrowing or gastric contour de- formity, were visualized. Other fold abnormalities representing neither prominence nor nodularity also were recorded. Gastric folds were prominent in 10 of 60 exam- inations (Table 2). In 1 case there was a question- able nodular defect in the distal antrum, and in 1 case there was a questionable antral polyp. In the control group, only 6 of 60 examinations presented with prominent folds, particularly within the antrum. There were no nodular defects within this Top) Good surface pattern of the stomach demonstrates group. Fig. 2A. ( sharpness of the areae gastricae pattern in a patient without renal The character of the fold pattern in the descend- failure. Fig. 2B. (Middle) Poor surface pattern in a patient with ing duodenum was assessed in the same manner as chronic renal failure and on dialysis illustrates poor mucosal was the gastric fold pattern, on the basis of an adherence of barium and no areae gastricae. Fig. 2C. ( Bottom) Fair surface pattern in a chronic renal failure patient on dialysis overall appearance produced by thickness, coarse- depicts a limited areae gastricae pattern without extensive pud- ness, and irregularity (Fig. 3). In 13 of the 60 exam- dling of barium.

Surface pattern of the stomach and duodenum in a chronic renal failure cohort 164/77 TABLE 1. SURFACE PATTERN OF THE STOMACH. studies had nodules measuring 1.5 cm., and in 1 Visualization examination there was a 2-cm. nodule (Fig. 4). In 11 of the 21 studies, more than 1 nodule was present in Cohort Poor Fair Good the cap (Fig. 5), while in the remaining 10 only a Renal failure 31 10 4 single nodule could be identified. Without renal failure 0 14 46 There were 37 examinations in which nodules in

TABLE 2. PROMINENT MUCOSAL FOLDS. the duodenal loop were visualized (Fig. 6). Of these, 32 presented more than 1 nodule, while 5 demon- Cohort Gastric fold Duodenal fold strated only a single defect. Twenty studies pre- Renal failure 10 13 Without renal failure 6 20 sented nodules that measured less than 6 mm. in diameter; 8 examinations revealed nodules be- tween 6 mm. and 1.0 cm., and in 9 examinations nodules larger than 1 cm. were observed (Table 4). In the control series, there were 6 cap nodules ranging in size from 3 mm.-1 cm. In 3 of 6 studies, there was more than 1 nodule. No duodenal loop nodules were found in these patients.

Ulcer The presence or absence of identifiable ulceration was recorded for both the stomach and duodenum. There were 2 gastric ulcers and 2 duodenal cap ulcers in the 60 renal failure examinations (Table 5). One of the patients with a cap ulcer had an ulcer scar in the gastric antrum. The control group, which included patients with complaints of peptic ulcer but without renal failure, displayed similar findings. In this group, there were 11 cap and 4 gastric ulcers.

Discussion At the end of 1980, about 52,400 patients were receiving dialysis in the United States, with the Fig. 3. Radiograph reveals prominence and irregularity of numbers increasing by 8,000 annually during the duodenal longitudinal loop folds in a patient with chronic preceding 8 years. 18-2° Another 4,700 patients un- renal failure on hemodialysis. derwent renal transplantation. Many of these pa- tients exhibit signs and/or symptoms of gastroin- testinal disorders during the course of their inations, it was thought that unusual fold disease, 21 and some of them are examined radi- prominence was present (Table 2). However, the ographically. In our institution, it is estimated that control group demonstrated prominent loop folds in 70-80 percent of end-stage renal disease patients 20 of 60 double-contrast examinations. are so examined. These statistics suggest that the appearance of the upper gastrointestinal tract in Nodular defects in duodenal cap and loop this group is of some importance in contemporary The surface and mucosal fold patterns of the duo- radiology. denal cap and loop were evaluated for the presence Several interesting features present themselves of nodular defects, as described previously. The for consideration as a result of this review. A com- number, distribution, and size of the defects were mon finding was the presence of nodular mucosal recorded. Of the 60 examinations, 21 presented defects, which fit the generally accepted descrip- duodenal cap nodules and 37 had identifiable duo- tion of hypertrophied Brunners glands, in the duo- denal loop nodules (Table 3). Fifteen studies re- denal cap and loop. Of the 60 examinations, 43 vealed coexistent cap and loop nodules. revealed at least 1 identifiable nodule. Authors The cap nodules ranged in size from 2 mm. to 2 have noted this phenomena in various contexts. cm.; most were in the 3-6 mm. range. Eight of the 21 Franzin and coworkers8 visualized hyperplastic studies revealed nodules larger than 6 mm., and 6 duodenal Brunners glands on in 26 of of these had 1 cm. or larger defects (Table 4). Two 102 renal failure patients. They saw histologic evi-

165/78 March 1986/Journal of AOA/vol. 86/no. 3 dence of hyperplasia of Brunners glands in duo- TABLE 3. DUODENAL NODULAR DEFECTS. denal biopsy material in 41 of 68 patients. Lewicki Location of defect and associates110 also described such a finding. Zuckerman and colleagues" reported similar find- Cohort Duodenal cap Duodenal loop Renal failure 21 37 ings; 14 of 17 patients with endoscopic duodenitis had histologic confirmation of an inflammatory in- Without renal failure 6 0 filtrate. However, Tani and coauthors did not de- Fifteen studies revealed coexistent cap and loop nodules. scribe visualization of hyperplasia in an analysis of endoscopic findings. In addition to the presence of nodules, their size, which in our series ranged up to 2 cm. in diameter, is notable. Of the 43 examinations with identifiable nodules, 6 patients presented lesions larger than 1 cm. The larger nodules could raise the question of neoplastic disease, and it is well to be aware of the level of expectation of their occurrence in this pa- tient cohort. The low incidence of identifiable ulceration sug- gests that peptic ulcer may not be a common prob- lem in dialysis patients. It is possible that the recognition of ulcer may be skewed in a group of double-contrast studies, most of which had a poor surface pattern. However, some of these were bi- phasic examinations, and a few were conventional single-contrast procedures. The literature varies widely in the reported incidence of ulcer in renal failure, from no demonstrated ulcers13,15,16 to a 53 percent incidence. 2 However, the majority of re- ports suggest a very low incidence of peptic ul- cers.11,22,23 The almost predictable occurrence of a poor gas- tric surface pattern in the standard double-con- trast procedure (31 of 45 examinations) raises some doubt as to the efficacy of the technique for gastric evaluation in dialysis patients. Ten of 60 examina- tions in our renal failure population underwent single-contrast studies because they were not able to tolerate the double-contrast procedure. But in these examinations, we were able to evaluate the gastric mucosa, duodenal cap and duodenal loop for the presence of nodules. Zuckerman and col- leagues" proposed that single-contrast barium ex- aminations were very accurate in depicting duodenal cap and duodenal loop nodules if the nod- ules were 5 mm. or larger in diameter. Approx- imately 50 percent of the upper gastrointestinal tract examinations had at least 1 nodule that was that large. Perhaps single-contrast studies would be more appropriate in the evaluation of these pa- tients. In the group without renal failure, 46 of 60 patients displayed good gastric surface patterns. Laufer) has demonstrated the importance of a good surface pattern within the stomach and duodenum Fig. 4. This 2-cm. nodule within duodenal cap ( arrows) in a for an accurate evaluation of ulcers. In the control chronic renal failure patient on hemodialysis was the largest nodule found in this series. Fig. 5. Roentgenogram depicts multi- group, 11 patients had duodenal ulcers and 4 had ple nodules ( arrows) and enlarged folds within a duodenal cap in gastric ulcers. Another 20 control patients dis- a patient with chronic uremia.

Surface pattern of the stomach and duodenum in a chronic renal failure cohort 166/79 maintenance dialysis cohort demonstrated a high incidence of nodular surface pattern defects in the duodenal cap and loop, a low incidence of identifi- able peptic ulcer, and a consistently poor gastric surface pattern. It is suggested that awareness of the presence of nodular defects and their possible size might be important in contemporary diag- nostic imaging, and that the double-contrast tech- nique might not be totally reliable for gastric evaluation in this patient group.

1. Laufer, I.: Upper gastrointestinal tract. Technical aspects. In Double contrast gastrointestinal radiology with endoscopic correlation. Ed. 1. W.B. Saunders Co., Philadelphia, 1979, pp. 59-77 2. Shepherd, A.M., Stewart, W.K., and Wormsley, K.G.: Peptic ulcera- tion in chronic renal failure. Lancet 1:1357-9, 16 Jun 73 3. Goldstein, D.A., et al.: The duodenal mucosa in patients with renal failure. Reponse to 1.25 I 01-112D3 . Kidney Int 19:324-31, Feb 81 4. Shapira, N.. et al.: Gastric mucosal permeability and secretion before and after hemodialysis in patients with chronic renal failure. Surgery 83:528-35, May 78 5. Mitchell, C.J., et al.: Gastric function and histology in chronic renal failure. J Clin Pathol 32:208-13, Mar 79 6. Ryabov. S.I., et al.: Present-day concepts on gastric pathology in pa- tients with chronic renal failure. Int Urol Nephrol 12:189-97, 1980 7. Tani, N., et al.: Lesions of the upper gastrointestinal tract in patients with chronic renal failure. Gastroenterol Jpn 15:480-4, 1980 8. Franzin, G., Musola, R., and Mencarelli, R.: Morphological changes of the gastroduodenal mucosa in regular dialysis uraemic patients. Histo- pathology 6:429-37, Jul 82 9. Dinoso, V.P., Jr., et al.: Gastric and pancreatic function in patients with end-stage renal disease. J Clin Gastroenterol 4:321-4, Aug 82 10.Lewicki. A.M., Saito, S., and Merrill. J.P.: Gastrointestinal bleeding in the renal transplant patient. Radiology 102:533-7, Mar 72 Fig. 6. Prominent nodules farrows/ and linear duodenal folds 11.Zuckerman, G.R., et al.: Nodular duodenitis. Pathologic and clinical are seen in a hemodialysis patient with chronic renal failure. characteristics in patients with end-stage renal disease. Dig Dis Sci 28:1018-24, 1983 TABLE 4 SIZE OF DUODENAL NODULAR DEFECTS IN RENAL 12. Ivy, A.C., Grossman, M.I., and Backrach, W.H.: Peptic ulcer. FAILURE EXAMINATIONS. Blakeston, Philadelphia, 1950, p. 608 13.Wiener, S.N., Vertes, V., and Shapiro, H.: The upper gastrointestinal Size tract in patients undergoing chronic dialysis. Radiology 92:110-4, Jan 69 14.King. A.Y., Schneider. H.J., and King, L.R.: The roentgen appearance Location Number of of the small bowel during long-term hemodialysis for chronic renal dis- of defect studies <6 mm. 6 mm.-1 cm. >1 cm. ease. Radiology 99:331-5, May 71 Duodenal cap 21 13 2 6 15.Margolis, D.M., et al.: Upper gastrointestinal disease in chronic renal Duodenal failure. Arch Intern Med 138:1214-7, Aug 78 loop 37 20 8 9 16.Smith, F.W., Petersen, J., and Junor, B.: The radiological assessment of gastric acid output in chronic renal failure. Clin Radiol 29:185-8, Mar 78 TABLE 5 ULCERS. 17. Dorph. S., et al.: Gastroduodenal mucosal changes in chronic Cohort Gastric ulcer Duodenal ulcer uraemia. Scand J Gastroenterol 7:589-92, 1972 18. Renal failure 2 2 Relman, A.S., and Rennie, D.: Treatment of end-stage renal disease (editorial). N Engl J Med 303:996-8, 23 Oct 80 Without renal failure 4 11 19.Vollmer, W.M., Wahl, P.W., and Blagg, C.R.: Survival with dialysis and transplantation in patients with end-stage renal disease. N Engl J Med 308:1553-68, 30 Jun 83 20. Burton. B.T.: The federal governments stake in uremia manage- ment. Diabetic Nephropathy 2:1-4, 1983 played prominent duodenal folds, probably as a 21.Griffiths, H.J.: The gastrointestinal system. In Radiology of renal failure, edited by H.J. Griffiths. Ed. 1. W.B. Saunders Co., Philadelphia, manifestation of the "nonspecific duodenitis" pat- 1976, pp. 156-78 tern of acid-peptic disease. Thus, in the population 22. Doherty, C.C., and McGeown, M.G.: Prevention of upper gastroin- testinal complications after kidney transplantation. Proc Eur Dial without renal failure, we believe that double-con- Transplant Assoc 15:361-71, 1978 trast examination remains the procedure of choice. 23. Doherty, C.C., et al.: Treatment of peptic ulcer in renal failure. Proc Eur Dial Transplant Assoc 14:386-95, 1977 Summary Retrospective evaluation of upper gastrointestinal tract examinations in an end-stage renal disease/ Accepted for publication in August 1985. Updating, as neces-

167 80 March 1986/Journal of AOA/vol. 86/no. 3 nary, has been done by the authors. the department. Dr. Scott is now in private practice and on the attending staff, Department of Radiology, Pottsville Hospital and Warne Clinic, Pottsville, Pennsylvania. At the time this paper was written, Dr. Scott was a resident in the Department of Radiology, Metropolitan Hospital-Central Dr. Scott, Pottsville Hospital, Department of Radiology, 420 Division, Philadelphia, where Dr. Rosenbaum was codirector of South Jackson Street, Pottsville, Pennsylvania 17901.

Surface pattern of the stomach and duodenum in a chronic renal failure cohort 168/81