POLYCYSTIC LIVER DISEASE: STUDIES ON THE MECHANISMS OF CYST FLUID FORMATION
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1 GASTROENTEROLOGY 66: , 1974 Copyright 1974 by The Williams & Wilkins Co. Vol. 66, No.3 Printed in U.S.A. POLYCYSTIC LIVER DISEASE: STUDIES ON THE MECHANISMS OF CYST FLUID FORMATION A case report JOHN FISHER, M,D., HAGOP MEKHJIAN, M.D., EDWARD L. C. PRITCHETT, M.D., AND LAWRENCE S. CHARME, M.D. Department of Medicine, Ohio State University Hospitals, Columbus, Ohio Analysis of cyst fluid in a patient with polycystic liver disease was carried out at the time of incidental abdominal surgery. Preoperatively administered bromosulfophthalein and 14C-cholic acid could not be demonstrated in cyst fluid. Close similarities were found between cyst fluid and plasma osmolarity and electrolyte concentrations, suggesting that the cyst lining may be freely permeable to inorganic ions. Although the exact mechanism of hepatic cyst enlargement remains obscure, the additional findings of albumin, immunoglobulins, and secretory component in the cyst fluid suggest that these molecules may play a role in cyst growth by acting as osmotically active organic substances. Since the description of polycystic liver disease by Bristowe in 1856,1 numerous theories have appeared regarding the pathogenesis of hepatic cyst formation. StilF was the first to suggest that cysts may arise from a developmental defect. After the work of' Moscowitz 3 8 years later the concept of maldevelopment during fetal life and failure of normal involution of the intrahepatic duct system has been generally accepted as a mechanism of cyst formation. Although several reports have shown the absence of bile pigments in hepatic cyst fluid,3-5 the pathophysiology of its formation remains unclear. Furthermore, published case reports 3-7 have not supplied information regarding the detailed composition of cyst fluid nor mechanisms of transport across the cyst wall. Such information may be important in our under- Received July 4, Accepted October 9, Address requests for reprints to: Dr. Hagop Mekhjian, Department of Medicine, Ohio State University Hospitals, 410 West 10th Avenue, Columbus Ohio standing of the clinical course of this disease. In this case, the diagnosis of polycystic liver disease was suspected prior to abdominal surgery for endometrial carcinoma. This circumstance provided an opportunity to study some aspects of the secretory capacity of hepatic cysts and to evaluate more fully the composition of the fluid obtained from them. Bromosulfophthalein (BSP) and cholic acid, which are normally actively secreted by the bile canaliculi,8, 9 did not appear in the cyst fluid. However, the finding of immunoglobulins A and G as well as secretory component suggest the presence of a "secretory" epithelium lining the cysts. Furthermore, the similarities between the ionic composition of cyst fluid and plasma suggest that this fluid may be accumulated by ultrafiltration. Case Report A 64-year-old woman was admitted to this hospital because of intermittent vaginal bleeding of 5-month duration. She had no other gynecological complaints since her last normal
2 424 FISHER ET AL. Vol. 66, No.3 menstruation at age 52 years. The patient's general health was good. Past records revealed a history of adult onset diabetes mellitus. Family history was negative for hepatic and renal disease as well as any congenital abnormalities. Physical examination revealed a healthy appearing, middle-aged woman. Blood pressure, pulse, and cardiopulmonary system were normal. The abdomen was flat, soft, and nontender. The liver was 14 cm in total length at the midclavicular line. It was smooth, firm, and nontender. No bruits were heard. No other abdominal masses were palpable. Pelvic examination was unremarkable except for bleeding from the external cervical os. Basic laboratory studies including hemoglobin, hematocrit, leukocyte count, urinalysis, urine culture, blood urea nitrogen, serum creatinine, electrolytes, serum glutamic oxaloacetic transaminase, serum glutamic pyruvic transaminase, lactate dehydrogenase, serum protein electrophoresis, icterus index, prothrombin time, calcium, and phosphorus were normal. Fasting blood sugars ranged between 148 and 255 mg per 100 ml. Forty-five minute BSP retention was 9 and 13% on two occasions. Liver scan revealed multiple filling defects consistent with either multiple cysts or neoplasm. Intravenous pyelogram was consistent with polycystic kidney disease. Endometrial biopsy revealed adenocanthoma of the uterus. Methods During surgery for removal of her pelvic tumor, hepatic cyst fluid was obtained. Eighteen hours prior to surgery 50 )J.C of HC-labeled cholic acid was fed to the patient with her evening meal. Forty-five minutes prior to the aspiration of the cyst fluid, BSP, 5 mg per kg, was injected intravenously. Three specimens of liver cyst fluid were obtained from separate cysts by aspiration through an 18 gauge needle. Simultaneous venous blood samples were also obtained. These specimens were either studied immediately on collection or frozen for later analysis. Aliquots of cyst fluid were then studied for the presence of BSP dye by the method of Seligson et al. 10; "C-cholic acid by scintillation spectrometry; and Na+, K+, Cl-, CO 2 -, urea nitrogen, sugar, and bilirubin using a Technicon AutoAnalyzer. Osmolarity was determined by freezing point depression, cholesterol by Leffler's method, II and protein electrophoresis using a Beckman Cellulose Acetate Unit. Analysis of simultaneous venous blood samples used identical methods. In addition, the following studies on cyst fluid were performed: bile acids were examined by thin layer chromatography; amino acid content was determined using a Technicon AutoAnalyzer l2 ; and protein immunoelectrophoresis was performed according to the method of Scheidegger. 13 Cultures of cyst fluid were carried out on routine aerobic and anaerobic media. Results At surgery the liver was enlarged. There were multiple cystic masses throughout its surface, varying in size from several millimeters to 2 to 3 cm in diameter. Wedge biopsy revealed several small cysts and a minimal increase in portal fibrosis (fig. 1). The cyst walls were lined with flat or low cuboidal epithelium (fig. 2). Other than the finding of glycogen nuclei, probably related to the patient's diabetes mellitus, the hepatic parenchyma appeared normal. Cultures for aerobic and anaerobic organisms were sterile. No formed elements were visualized on microscopic examination of the clear yellow cyst fluid. No evidence of 14C activity was found in any of the three cyst fluid samples, while a small amount of radioactivity was demonstrated in the serum samples (14 dpm per ml). While this level of radioactivity is rather small, it does suggest that absorption of bile salts occurred. Since the circulation of bile salts is limited primarily to the enterohepatic circulation, the low concentration in serum is not surprising. Simultaneous concentrations in bile would have been much greater than in serum and if any transport of I C across the cyst wall epithelium had occurred it would have been detected in the cyst fluid. Consistent with the absence of 14C in cyst fluid, thin layer chromatography failed to detect any unlabeled bile acids. Likewise, no BSP dye was found in any cyst sample while a simultaneous serum sample showed BSP retention of 18% (table 1). Since BSP and bile salts are probably transported by different carriers, their absence in cyst fluid suggests the lack of both transport mechanisms in the cyst membrane. Additional studies revealed an unexpectedly close similarity in osmolarity, urea nitrogen, and electrolytes between cyst
3 March 1974 POL YCYSTIC LIVER DISEASE 425 FIG. 1. Section of polycystic liver taken at the time of surgery. Two small cysts are shown with a single layer epithelial lining. The parenchyma shows glycogen nuclei, but is otherwise normal. fluid and serum (table 1). On the other hand, while blood sugar was 272 mg per 100 ml, cyst sugar remained below 10 mg per 100 ml in all three aliquots. A discrepancy between se.rum and cyst cholesterol levels was also.demonstrated (table 1). Only trace amounts of alkaline phosphatase, serum glutamic oxaloacetic transaminase, serum glutamic pyruvic transaminase, and lactate dehydrogenase activity were found in cyst fluid. However, a moderate amount of protein, 1.8 g per 100 ml of primarily albumin, was found. Protein immunoelectrophoresis further demonstrated the presence of IgG and IgA but did not demonstrate IgM. With the use of agar gel immunodiffusion, secretory component was also detected. Amino acid analysis showed only trace amounts of those constituents normally found in plasma. No unusual amino acids nor large amounts of a single amino acid were detected. Discussion Previous studies of polycystic disease of the liver have been concerned largely with the establishment of anatomical communications between hepatic cysts and the biliary tree. Studies by Beale 14 in 1856, and later by Hashemian and James 4 have suggested that dyes injected into the cyst cavity do not appear in bile. In our study, the failure to detect BSP or radioactivelabeled bile acids in the cyst fluid indicates that compounds known to be actively secreted by the biliary canaliculi are not components of cyst fluid. Although the possibility remains that the cyst wall epithelium at one time might have had the secretory characteristics of the biliary canalicular epithelium, the results from this case suggest that in the well formed cyst the epithelial lining does not functionally resemble biliary canalicular epithelium. Previous studies have not included a detailed analysis of the composition of hepatic cyst fluid. The similarities of electrolytes, urea, and osmolarity in plasma and cyst fluid found in this study suggest that the cyst fluid is in equilibrium with plasma, and that the cyst lining is freely permeable to inorganic ions. This concept
4 426 FISHER ET AL. Vol. 66, No.3 FIG. 2. View of the liver cyst lining showing monolayered low cuboidal epithelium. Variations in the size of the lining epithelium were dependent on the cyst size, with increasing flattening in larger cysts. TABLE 1. Comparison of components found in cyst fluid and simultaneous venous blood Serum Cyst 1 Cyst 2 Cyst 3 "C activity Present BSP" (%) Urea nitrogen (mg/ 100 m!) Na+ (meq/liter) K' (meq/liter) Cl- (meq/liter) CO, - Content Osmolarity Sugar (mg/loo ml) Cholesterol (mg/ 100 m!) a BSP, bromosulfophthalein. is supported by the previous demonstration that bile duct epithelium is permeable to Na 22 and K42.15 Furthermore, the absence of any appreciable amounts of glucose and cholesterol in spite of moderately high plasma levels suggests that the cyst lining is impermeable to larger molecules. In this respect, the cyst lining is similar to the epithelium of the large bile ducts A mechanism of bile salt-independent fluid secretion 18 may still be a factor in cyst fluid information and cannot be ruled out on the basis of this study. Enlarging cysts of the liver,19 as well as the kidney,20 generally do not become apparent until adult life. The explanation for this progressive enlargement is unknown. In view of the findings in this case, canalicular secretion does not appear to be a factor. Another possible mechanism is the generation of nondiffusible osmotically active organic substances. This mechanism has previously been suggested for the progressive enlargement of polycystic
5 March 1974 POL YCYSTIC LIVER DISEASE 427 kidneys.21 In contrast to studies of kidney cysts, however, this study detected only minute amounts of those amino acids normally found in plasma. These trace quantities are unlikely to have an important effect on osmotic equilibrium. On the other hand, an appreciable quantity of protein was demonstrated. A total concentration of 1.8 g per 100 ml of protein, primarily albumin, was found. Previous analyses of liver cyst fluid have demonstrated a wide range of protein concentrations, from 100 mg per 100 ml to 9.94 g per 100 ml. 19, 22 Although protein concentrations in normal bile are too negligible to be important osmotic components, 23 the quantities of protein found in most liver cyst fluids may have significance as nondiffusible charged particles. Since normal bile contains only insignificant quantities of protein, primarily albumin, the finding of relatively high concentrations of cyst fluid proteins, and the mechanism by which they reach the cyst fluid, needs explanation. It is possible that IgA and IgG found in this patient's cyst fluid could have resulted from transudation from serum. However, it is unlikely that secretory component could have resulted from such a process since it is synthesized separately from IgA, probably in glandular epithelial cells. 2 ' The mechanisms of liver cyst fluid formation have been largely speculative, The evidence from this patient confirms that no canalicular secretion exists. The findings of albumin in moderate concentration as well as IgA and secretory component suggest some capacity for epithelial secretion of proteins and their possible role in the progressive enlargement of cyst cavities. REFERENCES 1. Bristowe: Cystic disease of the liver, associated with a similar disease of the kidneys. Trans Pathol Soc Lond 7: , Still GF: Congenital cystic liver with cystic kid ney. Trans Pathol Soc Lond 49: , Moschowitz E: Non-parasitic cysts (congenital) of the liver, with a study of aberrant bile ducts. Am J Med Sci 131: Hashemian H, James TGI: Non-parasitic cysts of the liver. Br J Surg 42 : , Grime RT, Moore T, Nicholson A, et al: Cystic hamartomas and polycystic disease of the liver. Br J Surg 47: , Clagget OT, Hawkins WJ: Cystic disease of the liver. Ann Surg 123: , Saben G, Edwards GA: Polycystic liver disease with portal hypertension. Arch Intern Med 11: , Wheeler HO, Meltzer JI, Bradley SE: Biliary transport and hepatic storage of sulfobromophthalein sodium in the unanesthetized dog, in normal man, and in patients with hepatic disease. J Clin Invest 39: , Sperber I: Biliary secretion of organic anions and its influence of bile flow, The Biliary System. Edited by W Taylor. Oxford, Blackwell, 1965, p Seligson D, Marino J, Dodson E: Determination of sulfobromophthalein in serum. Clin Chern 3: , Left1er HH: Estimation of cholesterol in serum. Am J Clin Pat hoi 31: , Moore S, Stein WH: A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. J BioI Chern 211: , Scheidegger JJ: Une micro-methode de I'immunoelectrophorese. Intern Arch Allergy Appl Im- munol 7: , Beale L: Cystic disease of the liver, associated with similar disease of the kidneys-report of this specimen. Trans Pathol Soc Lond 7: , Chenderovitch J, Troupel S, Renault H. et al: Le transfert du Na" et du K" du sang dan la bile chez Ie coboye au cours de la cholerese a dobit bloque. Rev Fr Etudes Clin BioI 6: , Forker EL: Two sites of bile formation as determined by mannitol and erythritol clearance in the guinea pig. J Clin Invest '46: , Schanker LS, Hogben CA: Biliary excretion of inulin, sucrose and mannitol. Am J Physiol 200: , Preisig R, Cooper HL, Wheeler HO: The relationship between taurocholate secretion rate and bile production in the unanesthetized dog during cholinergic blockade and during secretin administration. J Clin Invest 41: , Comfort MW, Cray HK, Dahlin DC, et al: Polycystic disease of the liver: a study of 24 cases. Gastroenterology 20:60-78, Osathanondh V, Potter EL: Pathogenesis of polycystic kidneys. Type 3 due to multiple abnormalities of development. Arch Pathol 77: , Gardner KD: Composition of fluid in twelve cysts of a polycystic kidney. N Engl J Med 281: , Burch JC, Jones HE: Large nonparasitic cysts of
6 428 FISHER ET AL. Vol. 66, No.3 the liver simulating an ovarian cyst. Am J Obstet Gynecol 63: , Wheeler HO: Water and electrolytes in bile, Handbook of Physiology, sect 6: Alimentary Canal, vol 5. Edited by CF Code. Washington DC, American Physiological Society, 1968, p Tourville DR, Adler RH, Bienenstock J, et al: The human secretory immunoglobulin system. Immunohistological localization of A, secretory "piece," and lactoferrin in normal human tissues. J Exp Med 129: , 1969
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