Nodular Regenerative Hyperplasia of the Liver with and without Portal Hypertension: A Comparison
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1 ANNALS O F CLINICAL AND LABORATORY SCIEN CE, Vol. 16, No. 2 Copyright 1986, Institute for Clinical Science, Inc. Nodular Regenerative Hyperplasia of the Liver with and without Portal Hypertension: A Comparison AKIO HARADA, M.D., YASUNI NAKANUMA, M.D., SUGANTHA GOVINDARAJAN, M.D., and ROBERT L. PETERS, M.D. Department of Pathology, University of Southern California, Liver Unit, Rancho Los Amigos Medical Center, Downey, CA ABSTRACT The clinical and the pathologic features of seven patients with nodular regenerative hyperplasia of the liver are analyzed and com pared with those of 37 patients reported in the literature in an attem pt to distinguish the features of those with portal hypertension from those without. Severe degrees of obliterative portal venopathy usually associated with the portal hypertension w ere found among the various pathological features. The association of nodular regenerative hyperplasia with a variety of chronic diseases suggests a heterogeneous group of pathogenic mechanisms. Our study reveals that only some of these m echanism s lead to the hepatic changes that cause portal hypertension. Introduction unknown. Wanless et al14,15 have emphasized th a t in tra h e p a tic p o rtal venous lesions are im portant in the pathogenesis of hepatocytic hyperplasia as well as in the developm ent of portal hypertension. However, this mechanism is not applicable to all patients w ith N R H.13 Idiopathic portal hypertension (IPH) is also a non-cirrhotic liver disease in which there is no d iscern ib le cause of th e p o rtal hypertension except for varying rem nants of portal fibrosis. The aims of this study are (1) to identify any clinicopathologic differences b etw een th e p a tie n ts w ith N RH and portal hypertension and those with NRH only and (2) to identify any pathologic changes th at can be attrib u te d to the developm ent of portal hypertension /86/ $01.20 Institute for Clinical Science, Inc. N o d u lar re g e n e ra tiv e h y p e rp la sia (NRH) is a condition in which nodules of hyperplastic hepatocytes develop in a liv e r w ith a p re s e rv e d a rc h ite c tu a l framework.13 There is no fibrosis or cirrhosis. The etiology and pathogenesis of NRH remains unknown. Although a significant num ber of patients of NRH have portal hypertension and bleeding esophageal varices, the m echanism of portal hypertension in these patients remains Send reprint requests to Sugantha Govindarajan, M.D., USC Liver Unit, Pathology, Rancho Los Amigos Medical C enter, 7705 Golondrinas, 1200 Bldg., Downey, CA
2 156 HARADA, YAKANUMA, GOVINDARAJAN AND PETERS S uch a c o m p a ra tiv e stu d y w ith an emphasis on portal hypertension has not previously b een reported. O ur study includes seven p atien ts w ith NRH in whom either autopsies or wedge biopsy of the liver and adequate clinical data are available. In addition, all the reported cases of NRH in the literature are also included in the comparative analysis. Materials and Methods C l in ic o p a t h o l o g ic S t u d y Clinical data and liver tissues w ere available in seven patients with a diagnosis of NRH. Six of these patients were autopsied and one had wedge biopsy of liver. Liver biopsies from five of them were sent to one of the authors (RLP) for consultation, and th e rem ain in g two biopsies w ere from th e U niversity of Southern California Liver Unit Pathology D epartm ent. These patients fulfilled the criteria of NRH, originally described by Steiner et al.12 Four patients had evid en ces of p o rta l h y p e rte n sio n w ith eosphageal varices (group A), and the other three patients had no distinct evidence'of portal hypertension (group B). The histologic sections w ere stained with hematoxylin and eosin, and, when indicated, with Masson s trichrom e, elastic Van Gieson, and reticulum stains. The sections w ere carefully examined for the following histologic changes, which have been described in the literature in association w ith N R H 5' and idiopathic portal hypertension:1,8 sinusoidal dilatation, approximation of portal tracts, portal fibrosis, sclerosis of portal vein branches, old thrombosis of portal vein b ra n c h e s, d ila ta tio n o f p o rta l v ein branches, thickness of term inal hepatic vein branches, angiomatous vascularity in the portal tracts, periductal fibrosis, and anomalous arterial branches. Review of Literature and Comparative Study From 92 patients of NRH reported in the literature from 1953 to 1984, 37 who had portal hypertension w ere selected for th e stu d y. In c lu d in g th e se v en patients rep o rted here by the p resen t authors, a total of 44 patients were available for a comparative clinicopathologic study. Thirty-one patients had evidences of portal hypertension (group A), and the other 13 patients bad none (group B). E so p h ageal v arices, w ell d e v e lo p e d p o r to - s y s te m ic c o lla te r a ls a n d /o r increased m anom etric portal p ressu re w ere re g a rd e d as fe a tu re s o f p o rta l hypertension. Using the student s t test for paired variables, statistical com parisons were made. Results C l in ic o p a t h o l o g ic F in d in g s o f C u r r e n t S e v e n C a s e s F our patients w ere m ale and th ree w ere female. The average age was 52. Six patients had associated chronic disorders (table I). In general, th e liver w eig h ed less am ong th e p a tie n ts in group A than among those in group B. Gross findings in cases 4 and 5 showed variable sized whitish nodules in case 5 (figure 1) and tan miliary nodules in case 4. T he n odules revealed hep ato cy tic hypertrophy resulting in bulging areas, especially in zones 1 and 2 (figure 2). Approximation of portal tracts and obliterativ e changes of sm all p o rtal vein branches w ere more prom inent in group A (figures 3 and 4). M ajor portal vein branches revealed severe sclerosis and partial fibrous occlusive process in group A (figure 5). Sinusoidal dilatation (figure 2), phlebosclerosis, and dilatation of portal vein branches were, however, comm on featu res in both groups. Portal
3 157 NODULAR REGENERATIVE HYPERPLASIA TABLE I C lin ic a l D ata o f th e C u rre n t Seven Cases C ase Group A 1* A 2 A 3f A 4 A Group B 5 A 6 A 7 WB S e x /A g e M/45 M/78 M/50 F/43 F/41 M/54 F/52 A s s o c i a t e d C h r o n ic D is o r d e r s Post renal transplant None Connective tissue disorder Turner1s syndrome Diabetes mellitus with hypothyroidism E so p h a g e a l v a r ic e s U pper G I B le e d in g ND A s c ite s S p le n o m e g a ly Systemic lupus erythematosus Cardiomegaly Ulcerative proctosigmoiditis Reported case by Stromeyer, F.W. and Ishak, K.G.: Human Pathol. 12_:60-71, { Reported case by Wanless, I.R. et al: Medicine 59^ , A = Specimen from autopsy WB = Specimen from wedge biopsy ND = Not described fibrosis, angiomatous vascularity in the C o m p a r is o n o f portal tracts, periductal fibrosis, and C l in ic o p a t h o l o g ic F e a t u r e s anom alous a rte ria l b ra n c h e s w ere T he c o m p ariso n is b e tw e e n th e present in two or three patients irrespec patients with evidence of portal hyper tive of the presence of portal hyperten tension and those without and includes sion (table II). F igure 1. Cut surface of the autopsy liver shows various-sized whitish nod ules throughout the hepa tic parenchyma. Case 5.
4 158 HARADA, YAKANUMA, GOVINDARAJAN AND PETERS F ig u r e 2. Hyperplas tic nodules (arrows) of hepatocytes involve zone 1 and zone 2. The paren chyma betw een nodules shows hepatocytic atrophy and sinusoidal dilatation. Case 2. H&E x 80. the c u rre n t cases in th e lite ra tu re review. The data in table III show that the patients in group A were significantly younger than those in group B (p < 0.05). Although a variety of chronic dis orders was found in association with NRH, rheumatoid arthritis was the most common disease among the patients in group A. Cardiovascular diseases were more commonly seen among the patients in group B. A variety of hematologic dis orders were seen among patients in both groups. Seven patients in group A had no associated chronic disorders. The average weight of the liver of group A F ig u r e 3. Portal ve nous elem 'ents are not seen in a portal tract, sug gesting portal venous obli teration. Case 2. H&E x 400. was significantly sm aller than that of group B (p < 0.05). Sinusoidal dilatation and phlebosclerosis were found in some patients in group B as well as those in group A. Clustering of portal tracts and some areas of normal appearance were identified in some patients in group A. Discussion There are several hypotheses regard ing the pathogenesis of portal hyperten sion associated with NRH: (1) increased portal blood flow with splenomegaly;9 (2) distortion of compression of the intrahe-
5 NODULAR REGENERATIVE HYPERPLASIA 159 F igure 4. Portal tracts (arrow s) are a p p ro x i m a te d. T h e re is o ne hyperplastic nodule (left) a n d h e p a tic v e n o u s branch (upper center). Case 4. H&E x 80. patic vessels by the hyperplastic hepatocytic parenchyma;1013 (3) a combination of hypotheses 1 and 2;2 and (4) obliterative portal vein lesions by vascular dis ease or sluggish blood flow.1415 Some patients of NRH with portal hyperten sion have no splenom egaly, w hereas some with splenomegaly show no portal h y p e rte n sio n. T h e re fo re, it seem s unlikely that increased portal blood flow through the splenic vein is an essential causal factor of portal hypertension.8 The hypothesis of distortion or compression of the intrahepatic vessels seems appro priate because some reports described elevated wedged hepatic venous pres sure that indicated post-sinusoidal block ade;310 however, details of such mecha nism rem ain unclear. The concept of obliterative portal venopathy as a causal factor of portal hypertension by Wanless et al1415 was particularly interesting because sim ilar vascular lesions had been reported in IPH livers.1,8 F igu re 5. Major portal vein with severe sclerosis and partial fibrous occlu sion. Case 2. H&E x 100.
6 160 H A R A D A, Y A K A N U M A, G O V I N D A R A J A N A N D P E T E R S T A B L E II Pathologic Findings of the Liver in the Current Seven Cases G roup A Group B ( w i t h p o r t a l ( w i t h o u t p o r t a l h y p e r t e n s i o n ) h y p e r t e n s i o n ) Liver weight (g) 1100 NA NA (Bx) Sinusoidal dilatation Approximation of portal tracts - - Portal fibrosis Sclerosis of portal vein branches - Obliterative changes of portal vein branches - Old thrombosis of portal vein branches Dilatation of portal vein branches - - Thickness of terminal vein branches - (-) absent () present () striking degree of change NA = not available Bx = biopsy The presen t com parative pathologic study betw een the patients of NRH with and without evidence of portal hypertension reveal that the obliterative changes of intrahepatic portal vein branches, approximation of portal tracts, and thickening of term inal veins w ere frequently present in group A. Furtherm ore, there was a significant difference of the weight of livers betw een the patients in group A T A B L E III Clinicopathologic Data of 44 Cases of Nodular Regeneration Hyperplasia Group A (n = 31) G roup B (n = 13 ) ( w i t h p o r t a l h y p e r t e n s i o n ) ( w i t h o u t p o r t a l h y p e r t e n s i o n ) Sex (M:F) 14:17 5:8 Age (mean ± S.D.) 51.8 ± 18.6* 65.8 ± 15.1* Associated chronic Rheumatoid arthritis 9 Cardiovascular disorders 7 disorders (number Hematologic disorders 4 Hematologic disorders 6 of patients) Systemic lupus Carcinoma of the large erythematosus 2 intestine 2 Tuberculosis 2 Rheumatoid arthritis 1 Post renal transplant 2 Systemic lupus Diabetes mellitus 2 erythematosus 1 CRST syndrome 1 Polyarthritis nodosa 1 Pulmonary arterial Ulcerative proctohypertension 1 sigmoiditis 1 Connective tissue disease 1 Turner's syndrome 1 None 7 Liver weight (g) 1473 ± 675* (n = 14) 2090 ± 668* (n = 12) (mean ± S.D.) Histologic findings: Phlebosclerosis Sinusoidal dilatation Clustering of portal tracts Local areas of normal liver Phlebosclerosis Phlebothrombosis Sinusoidal dilatation *p < 0.05
7 and those in group B. T hese findings m ay s u g g e s t th a t th e o b lite r a tiv e ch an g es of in tra h e p a tic p o rta l v ein branches cause an atrophy of liver by reduction or insufficiency of portal blood flow,4 as well as the developm ent of portal h y p e rte n s io n. T h e liv e rs o f th e patients with IPH w ere also atrophic and show ed th ese histologic ch anges.1 8 It seem s p o ssib le, th e re fo re, th a t th e m echanism s of d ev elo p m en t of portal hypertension in the patients with NRH is sim ilar to th at in th e p atien ts w ith IP H. H ow ever, th e livers w ith IP H never show diffuse nodular formation, although they occasionally show focal h y p ertro p h ic n odules. T he reason is unknown. Klofkorn et al6 su g g ested th at th e occurrence of esophageal varices probably reflected the chronicity of the process of NRH. The present study did not support th e ir hypothesis because the patients of group A w ere significantly younger than those of group B, and some patients in group B had long-standing disorders. The chronicity of the process does not seem the principle factor of the developm ent of portal hypertension. A lth o u g h m o s t o f th e r e p o r t e d p atien ts w ith N R H have a variety of associated chronic diseases such as rheumatoid arthritis, extrahepatic neoplasms, hematologic, cardiovascular, and endocrine disorders, seven patients in this study lacked any obvious chronic diseases. The present study suggests that am ong the p atien ts w ith N R H, those with rheum atoid arthritis manifest evidence of portal hypertension more often than those w ith oth er types of chronic disorders. This means that several pathogenic processes may be operating in the developm ent of a single phenom enon, n o n -c irrh o tic n o d u la r h y p e rp la s ia throughout the liver. Thus, it is speculated by th e p re se n t authors th at the pathogenesis of NRH is probably multifactorial and the development of portal NODULAR REGENERATIVE HYPERPLASIA 161 hypertension in NRH depends on the underlying pathogenesis of NRH. Acknowledgments The authors are grateful to K. G. Ishak, M.D., Ph.D. in Washington, D.C., A. Lui, M.D. in San Pedro, CA., I. R. Wanless, M.D. in Toronto, Canada, J. G. Gregonis, M.D. in A uburn, CA and Y. S. F. Miao, M.D. in Fullerton, CA. for sending the liver specimens to one of the authors (RLP). References 1. A ik a t, B. K., B h u s n u r m a t h, S. R., C h u t t a n i, P. N., et al: The pathology of noncirrhotic portal fibrosis. A review of 32 autopsy cases. Hum. Pathol. 70: , B l e n d is, L. M., L o v e l l, D., B a r n e s, C. G. et al: Esophageal variceal bleeding in Felty s syndrom e associated with nodular regenerative hyperplasia. Ann. Rheum. Dis. 37: , B l e n d i s, L. M., P a r k in s o n, M. C., S iu l k i n, K. B., et al: Nodular generative hyperplasia of the liver in Felty s syndrome. Quart. J. Med. 43:25-32, B o y e r, J. L. and G a u t u m, A: Organized intrahepatic portal throm bi A heterogeneous syndrome resulting in idiopathic portal hypertension, p a re n c h y m a l a tro p h y an d n o d u la r regeneration. Idiopathic Portal Hypertension. Okuda, K. and Omata, M., eds. Tokyo, University of Tokyo Press, 1983, pp H a r r is, M., R a s h, R. M., and D y m o c k, I. W. : Nodular, non-cirrhotic liver associated with portal hypertension in a patient with rheumatoid arthritis. J. Clin. Pathol. 27: , K l o f k o r n, R. W., S t e i g e r w a l d, J. C., M i l l s, D. M., et al: Esophageal varices in Felty s syndrome. Arthritis Rheum. 19: , N a k a n u m a, Y., O h t a, G., and S a sa k i, K.: Nodular re generative hyperplasia of the liver associated with polyarteritis nodosa. Arch. Pathol. Lab. Med. i 08: , O k u d a, K., N a k \ s h im a, T., O k u d a ir a, M., et al: Liver pathology of idiopathic portal hypertension. Com parison w ith non-cirrhotic portal fibrosis of India. Liver 2: , R eism an, T., L ev i, J. U., Z eppa, R., et al: Noncirrhotic portal hypertension in F elty s syndrome. Am. J. Digest. Dis. 22: , R o u g ie r, P., D e g o t t, C., R u e f f, B., et al: Nodular regenerative hyperplasia of the liver. Report of six cases and review of the literature. Gastroenterology 75: , S h o r l e y, J., W e in b e r g, M. N., F r e n k e l, E. P., et al: Nodular regenerative hyperplasia of the liver in a case of myelofibrosis with extramedullary hematopoiesis and secondary portal venous hypertension. Am. J. Clin. Pathol. 72: , 1979.
8 162 HARADA, YAKANUMA, GOVINDARAJAN AND PETERS 12. St e in e r, P. E.: Nodular regenerative hyperplasia of the liver. Am. J. Pathol. 35: , S t r o m e y e r, F. W. and I s h a k, K. G.: Nodular transformation (nodular regenerative hyperplasia) of the liver. A clinicopathologic study of 30 cases. Hum. Pathol. 22:60-71, W a n l e s s, I. R., G o d w in, T. A., A l l e n, F., et al: Nodular regenerative hyperplasia of the liver in hematologic disorders: A possible response to obliterative portal venopathy. Medicine 59: , W a n l e s s, I. R., S o l t, C., K orta n, P., et al: Nodular regenerative hyperplasia of the liver in hematologic disorders: A possible response to obliterative portal venopathy. Medicine 59: , 1980.
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