Liver Cysts in Autosomal- Dominant Polycystic Kidney Disease: Clinical and Computed
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1 229 Errol Levine1 Larry 1. Cook1 Jared J. Grantham2 Received January ; accepted after revision March 22, Presented at the annual meeting of the American Roentgen Ray Society. Boston, April Department of Diagnostic Radiology Bell Memorial Hospital, University of Kansas College of Health Sciences and Hospital, Rainbow Blvd. at 39th St.. Kansas City. KS Address reprint requests to E. Levine. 2 Department of Medicine. Division of Nephrology. University of Kansas College of Health Sciences and Hospital, Kansas City. KS AJR 145: , August X/85/ American Roentgen Ray Society Liver Cysts in Autosomal- Dominant Polycystic Kidney Disease: Clinical and Computed Tomographic Study Hepatic CT findings were analyzed in 44 patients with autosomal-dominant polycystic kidney disease and were correlated with liver and renal function tests and liver, splenic, and renal CT volume measurements. CT showed many large liver cysts in 31.8% of patients, small liver cysts in 25%, and no liver cysts in 43.2%. Patients with many large cysts often showed increased liver volumes. Splenic volumes did not differ significantly in patients with and without liver cysts, suggesting that portal hypertension is rarely associated with cystic liver disease. There was no correlation between severity of liver involvement and extent of renal cystic disease as determined from urea nitrogen and creatinine levels and renal volumes. Liver function tests were normal except in two patients, one with a cholangiocarcinoma, which may have arisen from a cyst, and the other with an infected liver cyst and chronic active hepatitis. Accordingly, if liver function tests are abnormal, an attempt should be made to identify complications of polycystic liver disease such as tumor, cyst infection, and biliary obstruction. Such complications are rare but may be seen in patients whose lives are prolonged by dialysis and renal transplantation. CT is a useful method for detecting liver cysts and identifying patients at risk for these complications. Multiple liver cysts occur commonly in autosomal-dominant polycystic kidney disease and are generally considered to have little clinical significance [1, 2]. However, patients now survive longer owing to dialysis and renal transplantation, and liver involvement may sometimes lead to significant morbidity and mortality in the late stages of the disease [2, 3]. We retrospectively evaluated clinical records and abdominal computed tomographic (CT) scans of 44 patients with autosomaldominant polycystic kidney disease to determine the frequency and patterns of liver cysts and their influence on hepatic function. Materials and Methods Between January 1978 and June 1 984, 44 patients with autosomal-dominant polycystic kidney disease were evaluated by abdominal CT. All showed typical clinical [1 ] and CT [4] findings of the disorder. The group included 24 men and 20 women ranging in age from 20 to 71 years (mean age, 44.1 years). Indications for CT included abdominal pain in 22 patients, assessment of disease extent in 1 5, family screening in four, and unexplained deterioration of renal function in three. Twenty-five patients were examined by CT before and after intravenous infusion of 1 50 ml of 60% iothalamate meglumine (Conray). Nineteen had unenhanced CT scans only. Blood or serum values measured in all patients at the time of CT included urea nitrogen, creatinine, total bilirubin, alkaline phosphatase, total protein, albumin, aspartate aminotransferase, and cholesterol. Renal, hepatic, and splenic volumes were calculated from CT scans in all patients. From the liver CT findings, the 44 patients were subdivided into three groups: (1) no liver cysts, (2) small cysts (less than 3 cm in diameter) (fig. 1), and (3) multiple large liver cysts (more than 3 cm in diameter) (fig. 2). Clinical, blood chemistry, and CT data for the three groups were subjected to statistical analysis.
2 230 LEVINE ET AL. AJR:145, August 1985 Results Frequency and Characteristics of Liver Cysts Fig. 1 -Contrast-enhanced CT scan. Many small cysts in both lobes of liver. Liver cysts were detected in 25 (56.8%) of 44 patients (table 1). Nineteen (43.2%) of 44 patients had no hepatic cysts (group 1); 1 1 (25%) had small liver cysts (group 2) (fig. 1), and 1 4 (31.8%) had many large hepatic cysts (group 3) (fig. 2). On CT, cysts showed no predilection for any particular lobe or segment of the liver. Most cysts had smooth contours, distinct interfaces with adjoining parenchyma, and fluid attenuation values (-5 to +20H). None showed contrast enhancement. Most cysts could be seen on unenhanced scans, but the lesions were easier to identify on contrast-enhanced images because of surrounding parenchymal enhancement (fig. 2) and opacification of blood vessels. Cyst calcification was rare, being found in only one patient (fig. 2). No instances Fig. 2.-A, tkienhanced CT scan. Many large cysts producing marked liver enlargement (volume = 10,340 cm ). Residual liver parenchyma is seen as strands of increased density surrounding cysts. Two small foci of calcification are present in cyst (arrow). B, After contrast enhancement. Increase in density of residual liver parenchyma so that cysts are more clearly defined. TABLE 1 : Clinical, Blood Chemistry, and Volume Data in Patients with Autosomal-Dominant Polycystic Kidney Disease Grouped According to Presence or Absence and Sizes of Liver Cysts cknicai Mean Blood Chenstry, and Mean Volume Data Mean age ± SEM (years) 42.6 ± ± ± 2.8 No.ofmen No.ofwomen No. (%) with hypertension 1 0 (52.6) 7 (63.6) 9 (64.3) No. (%) undergoing dialysis 3 (1 5.8) 2 (1 8.2) 6 (42.9) Blood urea nitrogen ± SEM (mg/dl) 36.7 ± ± ± 10.6 Creatinine ± SEM (mg/dl) 3.8 ± ± ± 1.1 Total bilirubin ± SEM (mg/dl) 0.5 ± ± ± 0.3 Alkaline phosphatase ± SEM (IU/L) 72.8 ± ± ± 36.6 Total protein ± SEM (g/dl) 6.9 ± ± ± 0.2 Albumin ± SEM (g/dl) 4.2 ± ± ± 0.1 Aspartate aminotransferase ± SEM (lu/l) ± ± ± 4.3 Cholesterol ± SEM (mg/di) 182 ± ± ± 7.8 Mean renal volume ± SEM (cm3) 951 ± ± ± 191 Liver volume ± SEM (cm3) 1598 ± ± ± 741 Splenic volume ± SEM (cm3) 335 ± ± ± 51 Note-Group 1 patients had no hepatic cysts; group 2 had sinai (< 3 cm) hv& cysts; group 3 had multiple large (> 3 cm) liver cysts.
3 AJR:145, August 1985 LIVER CYSTS IN POLYCYSTIC KIDNEY DISEASE 231 of intrahepatic biliary dilatation were seen. No splenic or pancreatic cysts were found. cant and there was no significant association between severity of liver involvement (table 1) and gender (p > 0.05). Relation between the Occurrence of Liver Cysts and Patient Age Although patients with many large liver cysts (group 3) had a greater mean age (table 1 ) than those with small cysts (group 2) or no cysts (group 1), the difference was not statistically significant (p > 0.05, analysis of variance test). Liver cysts were uncommon in patients younger than 30 years (table 2). Relation between the Occurrence of Liver Cysts and Gender The 24 men had a mean age of 45.8 years (SEM ± 3.1), while the 20 women had a mean age of 42.5 years (SEM ± 2.5). Cysts occurred in 12 (50%) of 24 men and 13 (65%) of 20 women. The 12 affected men had a mean age of 49.8 years (SEM ± 3.2) and a mean liver volume of 2268 cm3 (SEM ± 224), while the 13 affected women had a mean age of 41.7 years (SEM ± 2.6) and a mean liver volume of 3045 cm3 (SEM ± 856). Normal liver volume is about 1493 cm3 (SD ± 230) [5]. None of the gender differences were statistically signifi- TABLE 2: Age and Prevalence of Liver Cysts in Patients with Autosomal-Dominant Polycystic Kidney Disease Age (Years) No. Examined by CT No. (%) with Liver Cysts (12.5) (80.0) (70.0) (66.7) (42.8), Total (56.8) Relation between Occurrence of Liver Cysts and Clinical Findings Clinically detectable liver enlargement occurred in nine (20.5%) of 44 patients, all in group 3. Five (1 1.4%) had symptoms referable to the liver, which included dull upper abdominal pain and abdominal distension resulting from liver enlargement. Relation between the Extents of Hepatic and Renal Cystic Disease Analysis of variance and chi-square tests showed no significant association between extent of hepatic cystic disease and severity of renal cystic disease (table 1). Indeed, some group 3 patients showed normal or mildly impaired renal function and normal-sized or slightly enlarged cystic kidneys (fig. 3). Normal renal volume is about 330 cm3 (SD ± 84) [6]. Effect of Liver Cysts on Liver and Splenic Volumes Mean liver volume (table 1) was significantly greater in patients with many large liver cysts (group 3) than in those with small cysts or no cysts (p < 0.01, analysis of variance test). Normal liver volume is about cm (SD ± 230) [5]. There were no significant differences among the three groups (table 1) in mean splenic volume (p > 0.05, analysis of variance test) suggesting that portal hypertension is rarely associated with cystic liver disease. Normal splenic volume is about 219 cm3 (SD ± 76) [5]. Effect of Liver Cysts on Liver Function Analysis of variance tests showed no significant relation (p > 0.05) between extent of hepatic cystic disease and abnor- Fig. 3.-Unenhanced CT scans. A, Many large liver cysts produce marked liver enlargement (volume = 9066 cm3). B, Cystic kidneys are slightly enlarged (mean renal volume = 371 cm3). Renal function studies were normal.
4 232 LEVINE ET AL. AJR:145, August 1985 Fig. 4.-Cholangiocarcinoma. Contrast-enhanced scan shows several cysts in right lobe of liver. Poorly defined low-density mass (arrowheads) involves left lobe and part of anterior segment of right lobe. Lower-density areas within mass are probably cysts surrounded by infiltrating tumor. Ascites is present (cursor); spleen is enlarged. malities of liver function tests (table 1 ). The findings indicate that liver cysts, even when multiple and diffuse, do not usually have a detectable adverse effect on liver function. Liver function tests were abnormal in only two (4.5%) of 44 patients. One had a nonresectable cholangiocarcinoma (fig. 4) and died of metastatic disease. The other had an infected liver cyst shown by ln oxine-labeled white blood cell scaning but not by CT. The infection responded to antibiotic therapy. However, liver function impairment persisted and was shown by liver biopsy to be due to chronic active hepatitis, probably viral in origin. Discussion Patients with autosomal-dominant polycystic disease present a wide spectrum of hepatic and renal involvement. Some patients have renal cysts only; others have liver cysts only; while others show variable degrees of both kidney and liver involvement [7-1 0]. These manifestations may result from variable expressivity of a single dominant gene [7, 9]. Alternatively, there may be two separate, but closely related genes for hepatic and renal polycystic disease, respectively [7, 9]. On histologic examination, the liver cysts are usually lined by cuboidal epithelium, similar in appearance to that lining the bile ducts [2]. It is generally believed that the cysts develop from cystic dilatation of aberrant bile ducts (Meyenburg complexes) that fail to establish connection embryologically with the larger interlobular bile ducts in the portal tracts [2, 3]. The cysts do not communicate with the biliary system, but the lining cells gradually secrete fluid into the cysts [11]. Although multiple renal cysts have been encountered in children with autosomal-dominant polycystic kidney disease, liver cysts are rarely encountered in childhood [1 2]. Liver cysts usually first become manifest late in the third or in the fourth decade (table 1 ) and develop later than renal cysts [3, 12]. Our study suggests that liver cysts are more common and extensive in women with polycystic kidney disease than in men, and that they develop earlier in women. Although the gender differences were not statistically significant because of the small size of the patient population, these trends have been confirmed by other workers [3]. The frequency of liver cysts in any studied patient population will be affected considerably by its age and gender composition as well as by whether autopsy, liver scintigraphy, sonography, or CT was used to detect liver cysts. With the use of CT, which is highly sensitive for detecting small liver cysts, the frequency of liver cysts in autosomal-dominant polycystic kidney disease varies between 57% (present study) and 74% [1 3]. Our study did not show any relation between frequency and extent of hepatic cysts and degree of renal cystic involvement (table 1). Support for this finding comes from the study of Grunfeld et al. [3] in which about 68% of 1 24 patients with polycystic kidney disease on dialysis had liver cysts, while liver cysts were present in about 61 % of 120 nondialyzed patients. The morbidity and mortality of autosomal-dominant polycystic kidney disease are largely attributable to the renal disease, although rupture of berry aneurysms of the circle of Willis may lead to patient death [1 ]. However, fatal liver complications are now being reported more frequently in patients with polycystic kidney disease whose lives have been prolonged by dialysis or renal transplantation [3]. Since liver function tests are usually normal even in the presence of profound cystic liver disease, abnormal liver function tests should suggest the development of such liver complications. Liver failure, portal hypertension, and bleeding esophageal varices rarely lead to serious morbidity or death in autosomaldominant polycystic kidney disease [ ]. Several patients with these complications have shown fibrosis or cirrhosis of liver parenchyma between cysts, suggesting that superimposed diseases rather than the liver cysts themselves are usually responsible. The correct diagnosis may require liver biopsy, as in one of our patients. Patients with extensive polycystic liver disease may develop jaundice as a result of extrinsic compression of the common hepatic duct by cysts in the porta hepatis [ ]. Percutaneous aspiration of the cysts under CT or sonographic guidance or surgical decompression of cysts may be necessary to relieve the jaundice [18, 19]. Infection of liver cysts is rare, presumably because the cysts do not communicate with the biliary system. However, cyst infection, which is usually due to Escherichia co/i, may cause progressive liver failure and patient death [3, 20-23]. The diagnosis is difficult since the clinical features are nonspecific. Radionuclide scanning with 11n oxine-labeled Ieukocytes appears to be the most useful available method for diagnosing liver cyst infection [22]. As in one of our patients, it may not be possible to distinguish an infected cyst from uncomplicated liver cysts on CT [23]. Massive hemorrhage occurs rarely in liver cysts and may require surgery [8].
5 AJR:145, August 1985 LIVER CYSTS IN POLYCYSTIC KIDNEY DISEASE 233 Cholangiocarcinomas occur rarely in patients with multiple liver cysts, and tumor origin from cysts has been shown in some patients [2, 3, 24-26]. CT was useful for demonstrating such a tumor in the present study (fig. 4). The possibility of cholangiocarcinoma should be considered in any patient with autosomal-dominant polycystic kidney disease with significantly abnormal liver function tests. ACKNOWLEDGMENT We thank Kenneth Gerald for performing statistical analyses of the data. REFERENCES 1. Grantham JJ. Polycystic renal disease. In: Earley LE, Gottschalk CW, eds. Strauss and Welt s diseases of the kidney, 3d ed. Boston: Little, Brown, 1979: Hartnett M, Bennett W. Extrarenal mainfestations of cystic kidney disease. In: Gardner KD, ed. Cystic diseases of the kidney. New York: Wiley, 1976: Grunfeld JP, Albouze G, Jungers P, et al. Liver changes and complications in adult polycystic kidney disease. Adv Nephrol 1985;14: Levine E, Grantham JJ. The role of computed tomography in the evaluation of adult polycystic kidney disease. Am J Kidney Dis 1981;1 : Henderson JM, Heymsfield SB, Horowitz J, Kutner MH. Measurement of liver and spleen volume by computed tomography. Radiology 1981;141 : Ishikawa I, Saito Y, Onouchi Z, et al. Development of acquired cystic kidney disease and adenocarcinoma of the kidney in glomerulonephritic chronic hemodialysis patients. C/in Nephrol 1980;14: Berrebi G, Erickson RP, Marks BW. Autosomal dominant polycystic liver disease: a second family. C/in Genet 1982;21 : Peltokallio V. Non-parasitic cysts of the liver: a clinical study of 117 cases. Ann Chir Gynaecol [Suppl] 1970;59[1 74]: Nono A. Polycystic disease of liver: an entity of its own or not? (letter). Clin Genet 1983;23: Dalgaard 0. Bilateral polycystic disease of the kidneys. Acta Med Scand [Suppl] 1957;1 58(328): Patterson M, Gonzalez-Vitale JC, Fagan CJ. Polycystic liver disease: a study of cyst fluid constituents. Hepatology 1982;2: Milutinovic J, Fialkow PJ, Audd TG, Agodoa LY, Phillips LA, Bryant JI. Liver cysts in patients with autosomal dominant polycystic kidney disease. Am J Med 1980;68: Segal AJ, Spataro RF. Computed tomography ofadult polycystic disease. J Comput Assist Tomogr 1982;6: Aatcliffe PJ, Reeders 5, Theaker JM. Bleeding esophageal varices and hepatic dysfunction in adult polycystic kidney disease. Br MedJ [Clin Res] 1984;288: DelGuercio E, Greco J, Kim KE, Chinitz J, Swartz C. Esophageal varices in adult patients with polycystic kidney and liver disease. N EngI J Med 1973;289: Katzen NG. Fatal hepatic polycystic disease (letter). Br Med J 1964;28: Howard AJ, Hanson AF, Delaney JP. Jaundice associated with polycystic liver disease; relief by surgical decompression of the cysts. Arch Surg 1976;111 : Ergun H, Wolf BH, Hissong SL. Obstructive jaundice caused by polycystic liver disease. Radiology 1980;136: Wittig JH, Burns A, Longmire WP. Jaundice associated with polycystic liver disease. Am J Surg 1978;136: Robson GB, Fenster LF. Fatal liver abscess develoing in a polycystic liver. Gastroenterology 1964;47: Clinicopathological conference. A case of polycystic disease of the liver and kidneys. Br Med J 1965;4: Gesundheit N, Kent DL, Fawcett HD, Effron MK, Maffly RH. Infected liver cyst in a patient with polycystic kidney disease. West J Med 1982;1 36: Bourgeois N, Kinnaert P, Vereerstraeten P, Schoutens A, Toussaint C. Infection of hepatic cysts following kidney transplantation in polycystic disease. World J Surg 1983;7: Willis RA. Carcinoma arising in congenital cysts of the liver. J Pathol 1943;55: Bloustein PA, Association of carcinoma with congenital cystic conditions of the liver and bile ducts. Am J Gastroenterol 1977;67: Azizah N, Paradinas FJ. Cholangiocarcinoma coexisting with developmental liver cysts: a distinct entity different from liver cystadenocarcinoma. Histopathology 19804:
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