Hepatic Atrophy-Hypertrophy Complex Dueto Echinococcus granulosus

Koray Karabulut, M.D., _Ilgin Ozden, M.D., Arzu Poyanlı, M.D., Orhan Bilge, M.D.,Yaman Tekant, M.D., Koray Acarlı, M.D., Aydın Alper, M.D., Ali Emre, M.D.,Orhan Arıogul, M.D.

Obstruction of a major hepatic vein, or major portal vein, or biliary tree branch causes atrophy of the relatedhepatic region, and frequently, hypertrophy in the remaining liverdthe atrophy-hypertrophy complex(AHC). Whether hydatid cysts can cause AHC is controversial. The records of 370 patients who underwentsurgery for hepatic hydatid disease between August 1993 and July 2002 were evaluated retrospectively. Ex-cluding six patients with previous interventions on the liver, AHC had been recorded in the operative notesof 16 patients (4.4%); for all patients, a cyst located in the right hemiliver had caused atrophy of the righthemiliver and compensatory hypertrophy of the left hemiliver. The computed tomography images of sevenpatients were suitable for volumetric analysis. The median (range) right and left hemiliver volumes were334 (0–686) ml and 1084 (663–1339) ml, respectively. The median (range) cyst volume was 392 (70–1363) ml. AHC due to Echinococcus granulosus was confirmed by objective volumetric analysis. The presenceof AHC should alert the surgeon to two implications. First, pericystectomy may be hazardous due to asso-ciation with major vascular and biliary structures. Second, in patients with AHC, the hepatoduodenal lig-ament rotates around its axis; this should be considered to avoid vascular injury if a common bile ductexploration is to be performed. ( J GASTROINTEST SURG 2006;10:407–412) � 2006 The Society for Sur-gery of the Alimentary Tract

KEY WORDS: Hydatid disease, Echinococcus granulosus, hepatic atrophy, hepatic hypertrophy, atrophy-hypertrophy complex

Obstruction of a major hepatic vein or major por-tal vein or biliary tree branch causes atrophy of therelated hepatic region.1–11 Because the liver has thecapacity to regenerate, atrophy of a large hepatic pa-renchymal mass is usually associated with compensa-tory hypertrophy of the remaining liverdtheatrophy-hypertrophy complex (AHC).1–11 Adequateportal flow is a prerequisite for hypertrophy.5

In the few reports of hepatic atrophy associatedwith Echinococcus granulosus, frequencies ranging be-tween 8.3% to 21% have been reported.3,6 In con-trast, neither atrophy nor hypertrophy wasmentioned in large series of E granulosus pa-tients.12–19 The absence of uniform and practical cri-teria for atrophy and the AHC may account for thesediscrepancies.

This study was performed to investigate the AHCassociated with E granulosus by objective volumetric

� 2006 The Society for Surgery of the Alimentary Tract

Published by Elsevier Inc.

measurements in computed tomography (CT)images.

PATIENTS AND METHODS

The records of 370 patients who underwent sur-gery for hepatic hydatid disease between August1993 and July 2002 were evaluated retrospectively.Six patients who had undergone percutaneous (n 5 2)or surgical intervention (n 5 4) on the liver wereexcluded from analysis.

AHC had been recorded in the operative notes of16 patients (4.4%) who had no history of interven-tion of the liver. The CT images of seven patientscould be evaluated by image analysis (films werenot available for six patients and were unsuitablefor three patients). Five patients were women andtwo patients were men; mean age was 42 years

From the Departments of General Surgery, Hepatopancreatobiliary Surgery Unit (K.K., I.O., O.B., Y.T., K.A., A.A., A.E. O.A.) and Radiology(A.P.), _Istanbul University, _Istanbul, Turkey.This work was supported by the Istanbul University Research Fund (Project No. BYP-790/17102 005).Reprint requests: _Ilgin Ozden, Alkent 2000 Yeditepe Sitesi, Dolphin 6 Daire 4, B€uy€ukcekmece 34900, _Istanbul, Turkey. e-mail: iozden@hotmail.com

1091-255X/06/$dsee front matter

doi:10.1016/j.gassur.2005.06.007 407

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Fig. 1. (A) An 8.2 cm stage V cyst in segments 7 and 8. (B) Marked right hemiliver atrophy isevident in the lower sections of the same patient. The gallbladder (asterisk) is at the border of the liver.

(range, 26–61). For all patients, a cyst located in theright hemiliver20 had caused atrophy of the righthemiliver and compensatory hypertrophy of the lefthemiliver. The cysts were staged according to thecriteria of Gharbi et al.21

The Scion image analysis program (Scion Image,version beta 4.0.2, Frederick, MD) available from theNational Institutes of Health (NIH) Web site wasused for volumetric analysis. The landmarks pro-posed by Mukai et al.22 were adopted. The followinglines and their projections were used in the upperand lower sections as appropriate: a line containingthe main trunk of the middle hepatic vein anda line passing from the middle of the gallbladderbed and center of the inferior vena cava.

Volumetric studies on healthy liver donors re-vealed that the volume of the left hemiliver may ap-proach that of the right hemiliver, but very rarelyexceeds it.23,24 Therefore, AHC was diagnosed whenthe left hemiliver volume was equal to or higherthan that of the right hemiliver.

RESULTS

The results of volumetric analysis are presented inTable 1. In all seven patients with films suitable forevaluation, the operative observations were con-firmed by objective volumetric analysis. The cystwas located in the right hemiliver. Right hemiliveratrophy and compensatory hypertrophy of the left

Vol. 10, No. 32006 Hepatic Atrophy-Hypertrophy in Hyatidosis 409

Fig. 2. A 7.5 3 8 cm cyst in the atrophic right hemiliver that ruptured into the biliary tree. An air bubbleis anterior to the lesion (arrow), and the neighboring bile ducts (arrowheads) are dilated. The right branchof the portal vein is amputated by the cyst. Marked left hemiliver hypertrophy is evident.

hemiliver were observed. The converse situation wasnot recorded in any patient.

Interestingly, cyst volume showed a very widerange. A large cyst (e.g., 1363 ml) could causeAHC by simply replacing the hepatic parenchyma,whereas a small cyst (e.g., 70 ml) could effect thesame result by vascular compression.

All patients were treated by drainage of the cavity.Unroofing was added in two patients and omento-plasty in one patient. One patient was lost to fol-low-up. Postoperative CT examinations wereperformed in six patients to detect possible recur-rences at various intervals after the operation. Nosignificant changes were detected in the volumes ofthe right and left hemilivers. This is probably be-cause the liver had undergone ‘‘ultimate remodel-ing,’’ that is, there was no stimulus for regrowth ofthe atrophied right hemiliver because the left hemi-liver had already compensated for the loss of paren-chymal mass.

DISCUSSION

To the best of our information, this is the firstdemonstration of AHC due to E granulosus by CTvolumetric analysis. The previous reports on AHCdue to hydatid disease are controversial.3,6,7 Lobaratrophy due to E granulosus was first reported byHueston in 1953.1 Postmortem examination of fourlivers revealed segmental atrophy due to compres-sion of the portal vein, hepatic artery, and bile ductby the cyst, and also hypertrophy in the remaining

liver.1 Ham,3 in a study on patients with liver atro-phy, listed hydatid disease along with hepatocellularcarcinoma and cholangiocellular carcinoma as themost frequent causes of hepatic atrophy. Atrophywas noted in 13 of the 61 patients (21%) in that sur-gical series. On the other hand, this phenomenon hasnot been mentioned at all in larger series with 100 to350 patients each.12–19 In some studies,1,8,25 com-pensatory hypertrophy was noted in all patientswith atrophy, whereas Hann et al.5 noted contralat-eral hypertrophy in only 30% of the cases. The dis-crepancies may be due to the limited number ofpatients in some studies, and more importantly, thelack of uniform and practical criteria for atrophy. Adefinition was not given at all by some authors,1,6,7,8

whereas others used impractical definitions such as‘‘50% volume reduction in the size of a recognizedanatomical segment or lobe.’’3–5,8 In the presentstudy using criteria based on volumetric analysis,AHC was observed in 4.4% of the patients. Thatvolumetric analysis could be performed in 7 of 16cases is a shortcoming. However, it must be empha-sized that operative observations were confirmed byobjective measurements in analysis in all cases.

An important discrepancy with the litera-ture1,3,5,7,8 is the absence of left-sided atrophy inthe present report. This probably stems from theoriginal method of data acquisition. In the presentstudy, the first step was to review the operative re-cords that describe the size and the appearance ofthe liver. Because the size of a ‘‘normal’’ left hemi-liver is extremely variable,23,24 it may be difficult to

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Fig. 3. (A) A stage 3 cyst filling the right hemiliver completely. (B) A more inferior section shows thatthe right branch of the portal vein (arrow) ends in the cyst. Displacement of the gallbladder (asterisk) andcolonic interposition occurred due to right hemiliver atrophy. Marked hypertrophy of the left hemiliveris evident.

appreciate left hemiliver atrophy intraoperatively un-less it is markedly shrunken and fibrotic. In contrast,in studies based primarily on CT images, importantsigns such as crowding of the intraparenchymal vascu-lature and bile ducts can be more readily detected.3,5,8

In other words, some cases of left-sided atrophy mayhave been overlooked in the present study.

The detection of AHC has two surgical implica-tions. First, AHC reflects that the cyst is tightly in-volved with one or more of the portal triadstructures or a major hepatic vein. Pericystectomyis an effective radical operation in selected patients.26

However, close association with major vascular andbiliary structures is a relative contraindication for

this operation.26 As is the case in the present report,conservative surgical procedures (i.e., drainage com-bined with various cavity management methods)should be preferred to avoid injury in patients withAHC.

Table 1. The results of volumetric analysis

Median (range) right hemiliver vol* 334 (0–686) mlMedian (range) left hemiliver vol 1084 (663–1339) mlMedian (range) right hemiliver

vol/left hemiliver vol ratio47% (0%–54%)

Median (range) cyst vol 392 (70–1363) ml

*Excluding the cyst.

Vol. 10, No. 32006 Hepatic Atrophy-Hypertrophy in Hyatidosis 411

Second, AHC markedly alters the hepatic anat-omy and causes rotation of the organ around theaxis of the hepatoduodenal ligament.4,27–30 Conse-quently, the hepatic artery, and even the portalvein, may move to a location anterior to the commonbile duct. This anatomical pitfall should be takeninto consideration to avoid vascular injury if com-mon bile duct exploration is performed for intrabili-ary rupture of the hydatid cyst.31

The diagnosis of atrophy and the associated hy-pertrophy depends heavily on consideration of thisphenomenon.3 The following points should be con-sidered in the evaluation of imaging studies3,5,8,28: (a)volume reduction or expansion in a liver section orhemiliverdhepatic venous anatomy has been foundmost useful for this purpose,8 (b) ‘‘crowding’’ of vas-culobiliary structures in a part of the liver (the possi-bly atrophic area), (c) the presence of ‘‘splaying’’ andenlargement of vascular and biliary structures ina part of the liver (the hypertrophied area).

Preoperative diagnosis of atrophy and associatedhypertrophy is important in choosing a safe surgicalapproach and avoiding vascular injury.

CONCLUSIONS

Hydatid disease should be considered as a cause ofAHC in endemic regions. The diagnosis of atrophydepends heavily on consideration of this phenome-non.3 This is important in choosing a safe surgicalapproach and avoiding vascular injury.

The authors thank Mr. Recai Tosun for technical assistance in thepreparation of the manuscript.

REFERENCES

1. Hueston JT. The production of liver lobe atrophy by hydatidcysts. Br J Surg 1953;41:427–431.

2. Schweizer W, Duda P, Tanner S, et al. Experimental atro-phy/hypertrophy complex (AHC) of the liver: Portal vein,but not bile duct obstruction, is the main driving force forthe development of AHC in the rat. J Hepatol 1995;23:71–78.

3. Ham JM. Lobar and segmental atrophy of the liver. World JSurg 1990;14:457–462.

4. Hadjis NS, Blumgart LH. Liver hyperplasia, hypertrophyand atrophy: Clinical relevance. In: Blumgart L, ed. Surgeryof the Liver and Biliary Tract. New York: Churchill Living-stone, 1988, pp 61–71.

5. Hann LE, Getrajdman GI, Brown KT, et al. Hepatic lobaratrophy: Association with ipsilateral portal vein obstruction.Am J Roentgenol 1996;167:1017–1021.

6. Haddad MC, Birjawi GA, Khouzami RA, Khoury NJ, El-Zein YR, Al-Kutoubi AO. Unilocular hepatic echinococcalcysts: Sonography and computed tomography findings.Clin Radiol 2001;56:746–750.

7. Ham JM. Segmental and lobar atrophy of the liver. SurgGynecol Obstet 1974;139:840–844.

8. Lorigan JG, Charnsangavej C, Carrasco CH, Richli WR,Wallace S. Atrophy with compensatory hypertrophy of theliver in hepatic neoplasms: Radiologic findings. Am J Roent-genol 1988;150:1291–1295.

9. Rozanes I, Acunas B, Celik L, Minareci O, Gokmen E. CTin lobar atrophy of the liver caused by alveolar echinococco-sis. J Comput Assist Tomogr 1992;16:216–218.

10. Lory J, Schweizer W, Blumgart LH, Zimmermann A. Thepathology of the atrophy/hypertrophy complex (AHC) ofthe liver. A light microscopic and immunohistochemicalstudy. Histol Histopathol 1994;9:541–554.

11. Balci NC, Tunaci A, Semelka RC, et al. Hepatic alveolarechinococcosis: MRI findings. Magn Reson Imaging 2000;18:537–541.

12. Yildirgan MI, Basoglu M, Atamanalp SS, et al. Intrabiliaryrupture in liver hydatid cysts: Results of 20 years’ experience.Acta Chir Belg 2003;103:621–625.

13. Alonso CO, Moreno GE, Loinaz SC, et al. Results of 22years of experience in radical surgical treatment of hepatichydatid cysts. Hepatogastroenterology 2001;48:235–243.

14. Gonzales EM, Selas PR, Martinez B, Garcia IG, Carazo FP,Pascual MH. Results of surgical treatment of hepatic hydati-dosis: Current therapeutic modifications. World J Surg1991;15:254–263.

15. Demirci S, Eraslan S, Anadol E, Bozatli L. Comparison ofthe results of different surgical techniques in the manage-ment of hydatid cysts of the liver. World J Surg 1989;13:88–91.

16. Kalovidouris A, Pissiotis C, Pontifex G, Gouliamos A,Pentea S, Papavassiliou C. CT characterization of multive-sicular cysts. J Comput Assist Tomogr 1986;10:428–432.

17. Beggs I. The radiological appearances of hydatid disease ofthe liver. Clin Radiol 1983;34:555–563.

18. Di Matteo G, Bove A, Chiarini S, et al. Hepatogastroenter-ology 1996;43:1562–1565.

19. Sayek I, Yalin R, Sanac Y. Surgical treatment of hydatiddisease of the liver. Arch Surg 1980;115:847–850.

20. The Brisbane 2000 terminology of hepatic anatomy andresections. HPB 2000;2:333–339.

21. Gharbi H, Hassine W, Brauner WN, Dupoch K. Ultrasoundexamination of hydatic liver. Radiology 1981;139:459–463.

22. Mukai JK, Stack CM, Turner DA. Pictorial essay. Imagingof surgically relevant hepatic vascular and segmental anat-omy. Part 1. Normal anatomy. Am J Roentgenol 1987;149:287–292.

23. Leelaudomlipi S, Sugawara Y, Kaneko J, Matsui Y,Ohkubo T, Makuuchi M. Volumetric analysis of liversegments in 155 living donors. Liver Transpl 2002;8:612–614.

24. Abdalla EK, Denys A, Chevalier P, Nemr RA, Vauthey JN.Total and segmental liver volume variations: Implications forliver surgery. Surgery 2004;135:404–410.

25. Takayasu K, Muramatsu Y, Shima Y, Moriyama N,Yamada T, Makuuchi M. Hepatic lobar atrophy after ob-struction of the ipsilateral portal vein from hilar cholangio-carcinoma. Radiology 1986;160:389–393.

26. Bilge O, Ozden I, Bilsel Y, et al. The role of total pericystec-tomy in hepatic hydatidosis. J Hepatobiliary Pancreat Surg1997;4:212–214.

27. William RJ, Blumgart LH. Operative repair of bile duct in-juries involving the hepatic duct confluence. Arch Surg 1999;134:769–775.

412 Karabulut et al.Journal of

Gastrointestinal Surgery

28. Hadjis NS, Adam A, Gibson R, Blenkharn JI, Benjamin IS,Blumgart LH. Nonoperative approach to hilar cancer deter-mined by the atrophy-hypertrophy complex. Am J Surg1989;157:395–399.

29. Blumgart LH. Hilar and intrahepatic biliary enteric anasto-mosis. Surg Clin North Am 1994;74:845–863.

30. Czerniak A, Soreide O, Gibson RN, et al. Liver atrophy com-plicating benign bile duct strictures: Surgical and interven-tional radiologic approaches. Am J Surg 1986;152:294–300.

31. Alper A, Arıogul O, Emre A, Uras A, Okten A. Choledocho-duodenostomy for intrabiliary rupture of hydatid cysts ofliver. Br J Surg 1987;74:243–245.