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Nodular duodenitis in chronic maintenance hemodialysis patients
0016·5107/85/3105·0318$02.00 GASTROINTESTINAL ENDOSCOPY Copyright © 1985 by the American Society for Gastrointestinal Endoscopy
Nodular duodenitis in chronic maintenance hemodialysis patients Jagdish C. Mangla, MD, FRCP(C), FACP Mark Pereira, MD Ajay Bhargava, MD Rochester, New York
A retrospective study of 138 cases of chronic hemodialysis between 1977 and 1982 were reviewed for endoscopic, radiographic, and histologic characteristics of duodenitis. Forty patients underwent upper gastrointestinal barium x-rays; 13 were found to have multiple duodenal bulb nodules and three of these patients had very prominent duodenal bulb folds. There were 42 patients on whom upper panendoscopy was performed, and multiple duodenal nodules were seen in 15 patients and thickened folds in three patients. There were five patients in whom nodules were seen only on endoscopy. The size of the nodules varied between 3 and 8 mm in diameter and mucosal folds between 4 and 8 mm. Duodenal mucosal hyperplasia with chronic inflammatory cell infiltrate was found on biopsy of the nodules in 12 cases, while three cases with nodules revealed blunted villous structure with chronic inflammatory cells.
Nonspecific duodenitis is a common disease entity, but nodular duodenitis is unusual. 1- 4 An increased incidence of duodenitis has been described in chronic renal failure. 5 The association of nodular duodenitis and end stage renal disease has only been recognized recently.s-s The present report describes our experience with nodular duodenitis in patients undergoing chronic maintenance hemodialysis (MHD) between 1977 to 1982. MATERIALS AND METHODS
The data on 138 patients in chronic MHD between 1977 and 1982 were reviewed. Upper gastrointestinal series or panendoscopy was done in 62 patients. The diagnosis of nodular duodenitis was made radiographically when two or more nodules were seen as filling defects in the duodenal lumen. On panendoscopy, nodules were considered significant when two or more nodules >3 mm in size were seen. Multiple biopsies were taken from nodules or hypertrophic folds. Serum gastrin and serum pepsinogen were measured in 29 patients. Serum gastrin was done by radioimmunoassay (Gastrin Immunotype Kit, Squibb & Sons, Inc., New York, N.Y.). The normal serum gastrin range is 50 to 300 pg/ml. Serum pepsinogens were assayed and reported as proteolytic From the University of Rochester, Monroe Community Hospital, Rochester, New York. Reprint requests: Jagdish C. Mangla, MD, Monroe Community Hospital, Gastroenterology Unit, 435 East Henrietta Road, P.O. Box 90S, Rochester, New York 14603. 318
units/24 hours of incubation as described by Mangla et al. 9 The normal serum pepsinogen level in this laboratory is 147 ± 20 units/24 hours of incubation. The data on 62 patients were analyzed (Tables 1 to 5). The mean age was 39 with a range of 22 to 68 years. The mean length of follow-up was 5 years. Nodules and prominent folds were located in the duodenal bulb. The number of nodules varied from 3 to 15 and the diameter of nodules was more than 3 mm. The mucosal fold had to be more than 4 mm thick to be considered a prominent fold. Figures 1 and 2 demonstrate endoscopic and radiological features of nodules and prominent folds. Most of the nodules revealed hyperplastic mucosa with chronic inflammatory cell infiltrate. Three cases showed a villous architecture, but the villi were short and broad with chronic inflammatory cell infiltration (Fig. 3). Most of the hypertrophic folds revealed mucosa with chronic inflammatory cell infiltrate. There was no evidence of any adenomatous growth or Brunner's gland hyperplasia. DISCUSSION
In MHD patients with nodular duodenitis, the nodules are located in the bulb and first part of the duodenum and number from 3 to 15. The nodules measure 3 mm or more in diameter and may be hyperemic, have erosions, and bleed easily. Nodules are more prominent when a concomitant duodenal ulcer is present. However, the ulcer may be hidden by the nodule. GASTROINTESTINAL ENDOSCOPY
Table 1. Nodules and prominent folds on upper gastrointestinal (UGI) series and endoscopy Total number of patients with endoscopy and/or x-ray Patients with UGI series only Multiple nodules seen on x-ray Prominent mucosal folds on x-ray Combined incidence of nodules plus folds on x-ray Patients examined by endoscopy Multiple nodules seen on endoscopy Thickened mucosal folds seen on endoscopy Incidence of nodules plus prominent folds seen on endoscopy Nodules seen on endoscopy missed on UGI series Patients with both endoscopy and UGI series
62 40 13 3 40% 42 15 3 42% 5 20
Nodular group· (N = 25)
Nonnodular group (N = 37)
12 2 2 10 5 5
13
Epigastric pain Anemia Dysphagia Hematemesis Nausea and vomiting History of ulcer Anorexia Guaiac-positive stool
Table 4. Radiological findings other than duodenal nodules
Duodenal ulcer Gastric ulcer Varices Esophageal stenosis Gastroesophageal reflux Normal
Nodular group· (N = 16)
Nonnodular group (N = 24)
5
6
1
1 1
o 1 2
7
2 5 17
• Nodular group includes patients with prominent folds.
Table 2. Presenting symptoms in 62 patients Presenting symptoms
correlation with histological findings is high. Zuckerman et al. 8 reported histological correlation in 82% of their cases of nodular duodenitis. The incidence of nodular duodenitis at routine endoscopy is only 4%.8 The correlation of histological findings with endoscopy in nonspecific duodenitis varies from 100%10 to
1 1
9 5 3 1 6
o 4
• Nodular group includes patients with prominent folds.
Table 5. Fasting serum gastrin and serum pepsinogen levels·
Mean gastrin (pg/ml) Range Mean pepsinogen tyrosine (units) Range
Nodular duodenum
Nonnodular duodenum
381 (151-1568)
412 (162-1728)
807.5
961
(256-2327)
(209-1948)
• The difference between the two groups was not statistically significant.
Table 3. Lesions other than duodenal nodules seen endoscopically in 42 patients Lesion Gastritis Esophagitis Duodenal ulcer Gastric ulcer Varices Antral erosions Pyloric stenosis Esophageal ulcer Normal
Nodular group· (N = 18)
Nonnodular group (N = 24)
3 5 7 1 1 3
4 5 3 2 2 4 1 2 3
6
• Nodular group includes patients with prominent folds.
The histological features of nodular duodenitis show focal chronic inflammatory cells and fibrinous infiltrate under the hypertrophic mucosa. The lamina propria is distorted due to edema. Nonspecific duodenitis is very difficult to diagnose at endoscopy, and the correlation of endoscopic findings with the histological picture is not good. 1O However, when nodules or prominent folds are present, the VOLUME 31, NO.5, 1985
Figure 1. The surface of the duodenal nodules has many erosions (arrows) on endoscopy. 319
Figure 2. Prominent folds on upper gastrointestinal series (arrows).
diarrhea, and gastrointestinal bleeding. 15-19 Peptic ulcer disease symptoms may vary from mild dyspepsia, severe pain, or upper gastrointestinal bleeding. A high incidence of hemorrhage from gastroduodenal ulcers and gastritis also occurs in transplant recipients. 2o The reasons for the increased incidence of upper gastrointestinal symptoms and lesions in uremia and MHD patients are not clearly understood. Earlier studies21 ,22 of chronically uremic patients reported hypo- or normochlorhydria, but more recent studies of maintenance dialysis patients show hyperchlorhydria. 17-19 There is poor correlation between gastric acid secretion and peptic ulceration. In a mixed population with varying degrees of renal function impairment, Mirsky et a1. 23 found that 71 % had abnormally high levels of serum pepsinogen. Although serum pepsinogen levels may be useful as an indicator or marker for peptic ulcer disease,24, 25 in MHD patients high serum pepsinogen levels may be the result of reduced renal function. The increased serum pepsinogen levels do correlate with the increased acid secretion found in some renal failure patients,17 implying a quantitative relationship between the chief and parietal cell mass, and serum pepsinogens in renal failure patients. 26 However, we could not find any correlation between gastrin, pepsinogen, and duodenal nodules.
REFERENCES 1. Weinstein W. The diagnosis and classification of gastritis and
Figure 3. This biopsy of a nodule shows broad hyperplasia with infiltration of chronic inflammatory cells of the villi (H & E, x300).
70%.11 Cotton et alY reported a correlation in only 44% and 57% of cases and demonstrated that 25% of patients with normal findings on endoscopy had an increased number of inflammatory cells in the lamina propria. Is there any importance to be attached to the finding of duodenitis? Jaffee and Laing13 followed 14 cases for 3 to 5 years and showed that six developed duodenal ulcers. In another study14 no ulcers were found in 39 cases followed for 6 months to 4 years. There were 10 cases of duodenal ulcer and three of gastric ulcer in our endoscopy group of 42 patients, giving a total incidence of 31 %, almost twice as high as that reported by Zuckerman et a1. 8 The patients on MHD have many gastrointestinal symptoms such as nausea, vomiting, 320
duodenitis. J Clin GastroenteroI1981;3(suppI2):1-7. 2. Gelzayd EA, Gelfand DW, Rinaldo JA. Nonspecific duodenitis: a distinct clinical entity? Gastrointest Endosc 1973;19:131-3. 3. Gelzayd EA, Biederman MA, Gelfand DW. Changing concepts of duodenitis. Am J Gastroenterol 1975;64:213-6. 4. Marzano CA, Fontan AN, Martiarena M, Piskorz E, Adami J, Rubio H. An attempt to correlate symptoms to bulbitis diagnosed by endoscopy. Scand J Gastroenterol 1979;14(suppl 54):23-4. 5. Dorph S, Oigaard A, Pederson G, McNair A, Sorensen MB. Gastroduodenal mucosal changes in uremia. Scand J Gastroenterol 1972;7:589-92. 6. Margolis DM, Saylor JL, Giesse G, DeSchryver K, Harter H, Zuckerman G. Upper gastrointestinal disease in chronic renal failure: a prospective evaluation. Arch Intern Med 1978; 138:1214-7. 7. Bhargava A, Mangla JC, Pereira M. Nodular duodenitis and its association with patients on chronic maintenance hemodialysis (abstract). Gastrointest Endosc 1983;29:165. 8. Zuckerman GR, Mills BA, Koehler RE, Siegel A, Harter HR, DeSchryver-Kecskemeti K. Nodular duodenitis-pathologic and clinical characteristics in patients with end-stage renal disease. Dig Dis Sci 1983;28(11):1018-24. 9. Mangla JC, Guarasci G, Turner MD. Simultaneous electrophoresis of pepsinogens and pepsins. Am J Dig Dis 1973;18:85764. 10. Gregg JA, Garabedian M. Duodenitis. Am J Gastroenterol 1974;61:177-84. 11. McCallum RW, Singh D, Wollman J. Endoscopic and histologic correlations of the duodenal bulb. Arch Pathol Lab Med 1979;113:169. 12. Cotton PB, Price AB, Tighe JR, Beales JWM. Preliminary evaluation of "duodenitis" by endoscopy and biopsy. Br Med J 1973;3:430-3. 13. Jaffe RH, Laing DR. Changes of the digestive tract in uremia:
GASTROINTESTINAL ENDOSCOPY
a pathologic anatomic study. Arch Intern Moo 1934;53:851-64. 14. Cheli R. What is new about duodenitis? Scand J Gastroenterol 1979;14(suppI54):28-30. 15. Swamy AP, Mangla JC, Cestero RVM, Guarasci G. Serum pepsinogens and gastrins in chronic hemodialysis patients. Biochem Moo 1981;25:227-33. 16. Schoenfeld PY, Humphreys MH. A general description of the uremic state. In: Brenner BM, Rector FC, OOs. The kidney. Philadelphia: WB Saunders, 1976:1423. 17. Shepard AMM, Stewart WK, Wormsley KA. Peptic ulceration in chronic renal failure. Lancet 1973;1:1357-9. 18. Bailey GL, Griffiths HL, Lock JP, Hampers CL, Merrill JP. In: Abstracts, American Society Nephritis, 5th Annual Meeting, 1971:5. 19. Ventkateswaran PS, Jeffers A, Hocken AG. Gastric acid secretion in chronic renal failure. Br Med J 1972;4:22-3. 20. Spanos PK, Simmons RL, Rattazzi LC, Kjellstrand CM, Buselmeier TJ, Najarian JS. Peptic ulcer disease in the transplant
VOLUME 31, NO.5, 1985
recipient. Arch Surg 1974;109:193-7. 21. Leiber CS, Lefeure A. Ammonia as a source of gastric hypoacidity in patients with uremia. J Clin Invest 1959;38:1271. 22. Samloff 1M, Liebman WM, Panitch NM. Serum group I pepsinogens by radioimmunoassay in control subjects with peptic ulcer. Gastroenterology 1975;69:83-90. 23. Mirsky lA, Futterman P, Kaplan S. Blood plasma pepsinogen II. The activity of the plasma from "normal" subjects, patients with duodenal ulcer, and patients with pernicious anemia. J Lab Clin Med 1952;40:188-9. 24. Spiro HM, Ryan AE, Jones CM. The relation of blood pepsin to gastric secretion with particular reference to anacidity and achylia. Gastroenterology 1956;30:563-79. 25. Rotter JI, Sones JQ, Samloff 1M, Richardson CT, Gursky JM, Walsh JH, Rimoin DL. Duodenal ulcer disease associated with elevated serum pepsinogen. I. N Engl J Moo 1979;300:63~. 26. Korman MG, Laver MC, Hansky J. Hypergastrinemia in chronic renal failure. Br Med J 1972;1:209-10.
321
Nodular duodenitis in chronic maintenance hemodialysis patients Jagdish C. Mangla, MD, FRCP(C), FACP Mark Pereira, MD Ajay Bhargava, MD Rochester, New York
A retrospective study of 138 cases of chronic hemodialysis between 1977 and 1982 were reviewed for endoscopic, radiographic, and histologic characteristics of duodenitis. Forty patients underwent upper gastrointestinal barium x-rays; 13 were found to have multiple duodenal bulb nodules and three of these patients had very prominent duodenal bulb folds. There were 42 patients on whom upper panendoscopy was performed, and multiple duodenal nodules were seen in 15 patients and thickened folds in three patients. There were five patients in whom nodules were seen only on endoscopy. The size of the nodules varied between 3 and 8 mm in diameter and mucosal folds between 4 and 8 mm. Duodenal mucosal hyperplasia with chronic inflammatory cell infiltrate was found on biopsy of the nodules in 12 cases, while three cases with nodules revealed blunted villous structure with chronic inflammatory cells.
Nonspecific duodenitis is a common disease entity, but nodular duodenitis is unusual. 1- 4 An increased incidence of duodenitis has been described in chronic renal failure. 5 The association of nodular duodenitis and end stage renal disease has only been recognized recently.s-s The present report describes our experience with nodular duodenitis in patients undergoing chronic maintenance hemodialysis (MHD) between 1977 to 1982. MATERIALS AND METHODS
The data on 138 patients in chronic MHD between 1977 and 1982 were reviewed. Upper gastrointestinal series or panendoscopy was done in 62 patients. The diagnosis of nodular duodenitis was made radiographically when two or more nodules were seen as filling defects in the duodenal lumen. On panendoscopy, nodules were considered significant when two or more nodules >3 mm in size were seen. Multiple biopsies were taken from nodules or hypertrophic folds. Serum gastrin and serum pepsinogen were measured in 29 patients. Serum gastrin was done by radioimmunoassay (Gastrin Immunotype Kit, Squibb & Sons, Inc., New York, N.Y.). The normal serum gastrin range is 50 to 300 pg/ml. Serum pepsinogens were assayed and reported as proteolytic From the University of Rochester, Monroe Community Hospital, Rochester, New York. Reprint requests: Jagdish C. Mangla, MD, Monroe Community Hospital, Gastroenterology Unit, 435 East Henrietta Road, P.O. Box 90S, Rochester, New York 14603. 318
units/24 hours of incubation as described by Mangla et al. 9 The normal serum pepsinogen level in this laboratory is 147 ± 20 units/24 hours of incubation. The data on 62 patients were analyzed (Tables 1 to 5). The mean age was 39 with a range of 22 to 68 years. The mean length of follow-up was 5 years. Nodules and prominent folds were located in the duodenal bulb. The number of nodules varied from 3 to 15 and the diameter of nodules was more than 3 mm. The mucosal fold had to be more than 4 mm thick to be considered a prominent fold. Figures 1 and 2 demonstrate endoscopic and radiological features of nodules and prominent folds. Most of the nodules revealed hyperplastic mucosa with chronic inflammatory cell infiltrate. Three cases showed a villous architecture, but the villi were short and broad with chronic inflammatory cell infiltration (Fig. 3). Most of the hypertrophic folds revealed mucosa with chronic inflammatory cell infiltrate. There was no evidence of any adenomatous growth or Brunner's gland hyperplasia. DISCUSSION
In MHD patients with nodular duodenitis, the nodules are located in the bulb and first part of the duodenum and number from 3 to 15. The nodules measure 3 mm or more in diameter and may be hyperemic, have erosions, and bleed easily. Nodules are more prominent when a concomitant duodenal ulcer is present. However, the ulcer may be hidden by the nodule. GASTROINTESTINAL ENDOSCOPY
Table 1. Nodules and prominent folds on upper gastrointestinal (UGI) series and endoscopy Total number of patients with endoscopy and/or x-ray Patients with UGI series only Multiple nodules seen on x-ray Prominent mucosal folds on x-ray Combined incidence of nodules plus folds on x-ray Patients examined by endoscopy Multiple nodules seen on endoscopy Thickened mucosal folds seen on endoscopy Incidence of nodules plus prominent folds seen on endoscopy Nodules seen on endoscopy missed on UGI series Patients with both endoscopy and UGI series
62 40 13 3 40% 42 15 3 42% 5 20
Nodular group· (N = 25)
Nonnodular group (N = 37)
12 2 2 10 5 5
13
Epigastric pain Anemia Dysphagia Hematemesis Nausea and vomiting History of ulcer Anorexia Guaiac-positive stool
Table 4. Radiological findings other than duodenal nodules
Duodenal ulcer Gastric ulcer Varices Esophageal stenosis Gastroesophageal reflux Normal
Nodular group· (N = 16)
Nonnodular group (N = 24)
5
6
1
1 1
o 1 2
7
2 5 17
• Nodular group includes patients with prominent folds.
Table 2. Presenting symptoms in 62 patients Presenting symptoms
correlation with histological findings is high. Zuckerman et al. 8 reported histological correlation in 82% of their cases of nodular duodenitis. The incidence of nodular duodenitis at routine endoscopy is only 4%.8 The correlation of histological findings with endoscopy in nonspecific duodenitis varies from 100%10 to
1 1
9 5 3 1 6
o 4
• Nodular group includes patients with prominent folds.
Table 5. Fasting serum gastrin and serum pepsinogen levels·
Mean gastrin (pg/ml) Range Mean pepsinogen tyrosine (units) Range
Nodular duodenum
Nonnodular duodenum
381 (151-1568)
412 (162-1728)
807.5
961
(256-2327)
(209-1948)
• The difference between the two groups was not statistically significant.
Table 3. Lesions other than duodenal nodules seen endoscopically in 42 patients Lesion Gastritis Esophagitis Duodenal ulcer Gastric ulcer Varices Antral erosions Pyloric stenosis Esophageal ulcer Normal
Nodular group· (N = 18)
Nonnodular group (N = 24)
3 5 7 1 1 3
4 5 3 2 2 4 1 2 3
6
• Nodular group includes patients with prominent folds.
The histological features of nodular duodenitis show focal chronic inflammatory cells and fibrinous infiltrate under the hypertrophic mucosa. The lamina propria is distorted due to edema. Nonspecific duodenitis is very difficult to diagnose at endoscopy, and the correlation of endoscopic findings with the histological picture is not good. 1O However, when nodules or prominent folds are present, the VOLUME 31, NO.5, 1985
Figure 1. The surface of the duodenal nodules has many erosions (arrows) on endoscopy. 319
Figure 2. Prominent folds on upper gastrointestinal series (arrows).
diarrhea, and gastrointestinal bleeding. 15-19 Peptic ulcer disease symptoms may vary from mild dyspepsia, severe pain, or upper gastrointestinal bleeding. A high incidence of hemorrhage from gastroduodenal ulcers and gastritis also occurs in transplant recipients. 2o The reasons for the increased incidence of upper gastrointestinal symptoms and lesions in uremia and MHD patients are not clearly understood. Earlier studies21 ,22 of chronically uremic patients reported hypo- or normochlorhydria, but more recent studies of maintenance dialysis patients show hyperchlorhydria. 17-19 There is poor correlation between gastric acid secretion and peptic ulceration. In a mixed population with varying degrees of renal function impairment, Mirsky et a1. 23 found that 71 % had abnormally high levels of serum pepsinogen. Although serum pepsinogen levels may be useful as an indicator or marker for peptic ulcer disease,24, 25 in MHD patients high serum pepsinogen levels may be the result of reduced renal function. The increased serum pepsinogen levels do correlate with the increased acid secretion found in some renal failure patients,17 implying a quantitative relationship between the chief and parietal cell mass, and serum pepsinogens in renal failure patients. 26 However, we could not find any correlation between gastrin, pepsinogen, and duodenal nodules.
REFERENCES 1. Weinstein W. The diagnosis and classification of gastritis and
Figure 3. This biopsy of a nodule shows broad hyperplasia with infiltration of chronic inflammatory cells of the villi (H & E, x300).
70%.11 Cotton et alY reported a correlation in only 44% and 57% of cases and demonstrated that 25% of patients with normal findings on endoscopy had an increased number of inflammatory cells in the lamina propria. Is there any importance to be attached to the finding of duodenitis? Jaffee and Laing13 followed 14 cases for 3 to 5 years and showed that six developed duodenal ulcers. In another study14 no ulcers were found in 39 cases followed for 6 months to 4 years. There were 10 cases of duodenal ulcer and three of gastric ulcer in our endoscopy group of 42 patients, giving a total incidence of 31 %, almost twice as high as that reported by Zuckerman et a1. 8 The patients on MHD have many gastrointestinal symptoms such as nausea, vomiting, 320
duodenitis. J Clin GastroenteroI1981;3(suppI2):1-7. 2. Gelzayd EA, Gelfand DW, Rinaldo JA. Nonspecific duodenitis: a distinct clinical entity? Gastrointest Endosc 1973;19:131-3. 3. Gelzayd EA, Biederman MA, Gelfand DW. Changing concepts of duodenitis. Am J Gastroenterol 1975;64:213-6. 4. Marzano CA, Fontan AN, Martiarena M, Piskorz E, Adami J, Rubio H. An attempt to correlate symptoms to bulbitis diagnosed by endoscopy. Scand J Gastroenterol 1979;14(suppl 54):23-4. 5. Dorph S, Oigaard A, Pederson G, McNair A, Sorensen MB. Gastroduodenal mucosal changes in uremia. Scand J Gastroenterol 1972;7:589-92. 6. Margolis DM, Saylor JL, Giesse G, DeSchryver K, Harter H, Zuckerman G. Upper gastrointestinal disease in chronic renal failure: a prospective evaluation. Arch Intern Med 1978; 138:1214-7. 7. Bhargava A, Mangla JC, Pereira M. Nodular duodenitis and its association with patients on chronic maintenance hemodialysis (abstract). Gastrointest Endosc 1983;29:165. 8. Zuckerman GR, Mills BA, Koehler RE, Siegel A, Harter HR, DeSchryver-Kecskemeti K. Nodular duodenitis-pathologic and clinical characteristics in patients with end-stage renal disease. Dig Dis Sci 1983;28(11):1018-24. 9. Mangla JC, Guarasci G, Turner MD. Simultaneous electrophoresis of pepsinogens and pepsins. Am J Dig Dis 1973;18:85764. 10. Gregg JA, Garabedian M. Duodenitis. Am J Gastroenterol 1974;61:177-84. 11. McCallum RW, Singh D, Wollman J. Endoscopic and histologic correlations of the duodenal bulb. Arch Pathol Lab Med 1979;113:169. 12. Cotton PB, Price AB, Tighe JR, Beales JWM. Preliminary evaluation of "duodenitis" by endoscopy and biopsy. Br Med J 1973;3:430-3. 13. Jaffe RH, Laing DR. Changes of the digestive tract in uremia:
GASTROINTESTINAL ENDOSCOPY
a pathologic anatomic study. Arch Intern Moo 1934;53:851-64. 14. Cheli R. What is new about duodenitis? Scand J Gastroenterol 1979;14(suppI54):28-30. 15. Swamy AP, Mangla JC, Cestero RVM, Guarasci G. Serum pepsinogens and gastrins in chronic hemodialysis patients. Biochem Moo 1981;25:227-33. 16. Schoenfeld PY, Humphreys MH. A general description of the uremic state. In: Brenner BM, Rector FC, OOs. The kidney. Philadelphia: WB Saunders, 1976:1423. 17. Shepard AMM, Stewart WK, Wormsley KA. Peptic ulceration in chronic renal failure. Lancet 1973;1:1357-9. 18. Bailey GL, Griffiths HL, Lock JP, Hampers CL, Merrill JP. In: Abstracts, American Society Nephritis, 5th Annual Meeting, 1971:5. 19. Ventkateswaran PS, Jeffers A, Hocken AG. Gastric acid secretion in chronic renal failure. Br Med J 1972;4:22-3. 20. Spanos PK, Simmons RL, Rattazzi LC, Kjellstrand CM, Buselmeier TJ, Najarian JS. Peptic ulcer disease in the transplant
VOLUME 31, NO.5, 1985
recipient. Arch Surg 1974;109:193-7. 21. Leiber CS, Lefeure A. Ammonia as a source of gastric hypoacidity in patients with uremia. J Clin Invest 1959;38:1271. 22. Samloff 1M, Liebman WM, Panitch NM. Serum group I pepsinogens by radioimmunoassay in control subjects with peptic ulcer. Gastroenterology 1975;69:83-90. 23. Mirsky lA, Futterman P, Kaplan S. Blood plasma pepsinogen II. The activity of the plasma from "normal" subjects, patients with duodenal ulcer, and patients with pernicious anemia. J Lab Clin Med 1952;40:188-9. 24. Spiro HM, Ryan AE, Jones CM. The relation of blood pepsin to gastric secretion with particular reference to anacidity and achylia. Gastroenterology 1956;30:563-79. 25. Rotter JI, Sones JQ, Samloff 1M, Richardson CT, Gursky JM, Walsh JH, Rimoin DL. Duodenal ulcer disease associated with elevated serum pepsinogen. I. N Engl J Moo 1979;300:63~. 26. Korman MG, Laver MC, Hansky J. Hypergastrinemia in chronic renal failure. Br Med J 1972;1:209-10.
321