J Clin Ultrasound 24:297-303, JulyiAugust 1996 0 1996 by John Wiley & Sons, Inc. CCC 0091-27511961060297-07

“Congealed Waterlilly” Sign: A New Sonographic Sign of Liver Hydatid Cyst

Durr-E-Sabih, MBBS,* Zahida Sabih, MBBS,* and A.N. Khan, FRCP, FRCRt

Abstract: The ultrasonographic (US) appearance of hydatid liver disease is well es- tablished, but solid cysts have long defied US characterization. We present 23 solid cysts and describe a new feature called the “Congealed waterlilly” sign. As the phys- ical characteristics of the hydatid fluid change from watery to a viscid gel, it becomes echogenic. The intact folds of the germinal layer trapped within the viscid matrix give rise to the appearance of curvilinear structures which no longer move with changing patient posture. Similar findings have been observed in eight medically treated pa- tients. We observed progression from an initial simple cyst to a “floating waterlilly” through to a “congealed waterlilly” in treated patients. The final appearance was in- distinguishable from the untreated solid cysts. The congealed waterlilly sign is reliable and strongly suggestive of hydatid cysts. 0 1996 John Wiley & Sons, Inc. Indexing Words: Echinococcus grunulosis . Liver cysts . Hydatid cysts, solid

Echinococcus granulosus is endemic t o many parts of the world. The liver is the most common organ involved where it presents as benign cysts. Echinococcal liver cysts have no typical symp- toms; diagnosis rests on a high index of clinical suspicion. Many lesions are diagnosed incidently with imaging

The appearance of hydatid liver disease in so- nography or computed tomography is character- istic only when daughter cysts or a detached membrane undulating in a cystic cavity are seen. The sensitivity of serological tests for hydatid is 78% to 94%, depending on the criteria for positiv- ity and the method

We present our experience with 23 solid hy- datid cysts which can be described as fairly char- acteristic, as we know of no other pathology that has a similar appearance. This was a serendipi- tous finding made while treating hydatid liver disease with high doses of mebendazole in 1986, and following up the doses ultrasonically. We noted that, with loss of intracystic pressure dur- ing therapy, the germinal layer falls away from

From the *Atomic Energy Medical Centre, Nishtar Hospital, Multan, Pakistan; and tNorth Manchester General Hospital, Manchester, UK. For reprint requests contact Dr A.N. Khan, North Manchester General Hospital, Manchester M8 6RL, UK.

the pericyst and there appears a sonographic “wa- terlilly” sign.” With further treatment, the cysts become smaller and the germinal layer more closely packed. The intervening matrix becomes echogenic and the membranes no longer move with change in the patient’s position. We call this a “congealed waterlilly” sign. We have since seen this pattern in untreated patients who presented for the first time to our institution on whom scans were performed for reasons unrelated to sus- pected hydatid liver disease.

MATERIALS AND METHODS

Between December 1988 and May 1993 we diag- nosed 217 liver hydatid cysts. Of these, 23 were solidified at presentation. The patients were 14 men and 9 women with ages ranging from 28 to 59 years. All 217 patients presented with non- specific symptoms, but all came from a highly en- demic area. The symptoms included right upper- quadrant discomfortlpain, nausea, vague indiges- tion, and loss of appetite.

The most clinically evident sign was hepato- megaly of varying degree; most were referred for suspicion of biliary disease. Twenty cases had sin- gle (solidified) cysts in the liver, two cases had two cysts (in each of these one cyst was “solidi-

297 VOL. 24, NO. 6, JULYiAUGUST 1996

SABIH ET AL.

fied” and the other had a complex appearance with both solid and cystic areas), and one case had two liver cysts and multiple peritoneal cysts. (The liver cysts showed a “solidified” pattern in one cyst and a complex pattern with both solid and multiple cystic areas in the other cyst.) Surgical confirmation was available in 18 patients, but 5 patients refused surgery. All ultrasound exami- nations were done using a digital, real-time scan- ner (General Electric, RT 3000). Linear or sector probes (3.5 MHz and 5 MHz) were used as appro- priate.

RESULTS

The common sonographic feature in all cases was a regular, round-to-oval shaped, well-defined le- sion with a variable background echogenicity, ranging from hypoechoic to hyperechoic with liver tissue. Superimposed on this background were multiple well-defined curvilinear struc- tures; these showed a central echogenic line sur- rounded on both sides by hypoechoic bands (rem- iniscent of collapsed stomach echoes) (Figure 1).

These curvilinear structures could be relatively straight or be folded upon themselves.

Nine cases had peripherally distributed cysts within the primary lesion. The background ma- trix was usually heterogeneous and had a number of echogenic foci within, which were of different sizes. In some cases the foci were arranged to form coarse streaks. Gross pathological correlation was available in 11 of the 18 patients who had sur- gery. The pericysts were markedly thickened and fibrotic. The inner walls were irregular showing hemorrhagic areas and pale segments revealed to be areas of necrosis on microscopy. The cyst con- tents were thick, yellow, and gelatinous with par- ticulate matter representing membranes. No via- ble protoscolices were found. No attempts were made to cultivate the fluid.

DISCUSSION

The presence of peripheral cysts with a central solid area in a well-defined lesion is taken to be suggestive of hydatids by some investigators,”

FIGURE 1. Fairly well-defined 8.1-cm complex mass within the right lobe of the liver with superimposed curvilinear echogenic streaks surrounded by hypoechoic bands.

298 JOURNAL OF CLINICAL ULTRASOUND

LIVER HYDATID CYST

FIGURE 2. Series of real-time ultrasonograms showing echographic changes in a liver hydatid cyst following an 8-week course of albdendazole. The cyst has been followed for 8 years. (A) Longitudinal scan through the right lobe of the liver showing a well-defined 9.2-cm cystic lesion with a small amount of debris. Initial scan performed 27 April 1986

but totally solidified lesions have posed diagnos- tic problems for so no lo gist^.^^"^^^

We believe that, as the physical characteristics of the hydatid fluid change from a water consis- tency to a viscous gel-like substance, it becomes more echogenic. We have no data indicating this effect, but increased echogenicity in liver ab- scesses has been described because of increased protein/lipid ~ 0 n t e n t . l ~ A similar mechanism may be involved in hydatid cysts transforming into solid cysts.

The intact folds of the germinal layer trapped in the viscous matrix give rise to the appearance of curvilinear structures. The coarse streaks formed by echogenic foci probably represent par- tially degenerated folds of the germinal layer. With further degeneration only focal areas of the germinal layer might remain, accounting for the echogenic foci.

A similar appearance was described by Ilter et a1 in 1985.14 They called the appearance of a “ball of wool” or a “yarn” sign. However, they did not

VOL. 24, NO. 6, JULYiAUGUST 1996

comment on the echogenicity of the intervening matrix, nor did they regard the sign as being spe- cific for liver hydatid cysts. They postulated that this appearance was due to the separation of the germinal layer from the inner side of the cyst and folding several times in a limited space. Garcia et all5 found that 17% of intra-abdominal hydatids were solid, among these one third presented with linear structures representing fragmented or in- folding membranes within a round or oval mass. They described these findings as highly charac- teristic of hydatid.

A “Spin” or “Whirl” sign, representing col- lapsed parasitic membranes, has been recognized in untreated liver hydatid by von Sinnor.“ This sign was considered strong evidence of hydatid disease even if the serological tests were unavail- able or falsely negative. Sanset et all7 described an‘lecho-free peritumoral collar” and an “echo- free spiral” as signs suggestive of hydatid disease. These signs correspond to peripherally placed daughter cysts and fragmented in-folded mem-

299

SABIH ET AL.

FIGURE 2. (B) Ultrasound scan on 24 August 1986 following treatment with albendazole. A ”floating waterlilly” sign has appeared (the germinal layer has fallen away from the pericyst).

branes respectively. It is possible that such an appearance may be related to degeneratingldead echinococcus granulosus.

Serological tests currently available would probably not be appropriate in this situation to assess activity, because these tests show either increase or decrease following treatment with mebendazole independent of the outcome of the parasitic disease.6 In our present state of knowl- edge we are not certain whether a “congealed wa- terlilly” represents a dead parasite and how many of these will eventually calcify. The fact that a similar appearance occurs with successful meben- dazole/albendazole treatment suggests that this is a healing process and eventually these cysts may become sterile. However, follow-up scans of liver hydatid after commencement of mebenda- zole/albendazole has shown transformation from cystic to echogenic appearance with reappearance of the daughter cyst after variable periods of ther- apy? The reappearance of daughter cysts during treatment with mebendazole has subsequently been treated with albendazole with successful re- sults.gJsJ9

300

However, the reappearance of hepatic cysts in patients who have undergone medical treatment in the past does not necessarily mean that these cysts are viable and alive.20 We postulate that a “congealed waterlilly” sign is a stage of relative inactivity or may represent a dead parasite, whether following medical treatment or occur- ring spontaneously. Even when armed with the knowledge of this finding, in some of the cases the degenerative process might have advanced too far to be recognizable even as coarse streaks, and these might be seen as amorphous solid masses indistinguishable from other solid lesions.

We present a series of scans (Figures 2A-2F) from a patient who has been treated with alben- dozole and followed-up for the last 8 years. The images show the progression from an initial sim- ple cyst to the “floating waterlilly” to the “con- gealed waterlilly” stage, and finally, at present having an amorphous echogenic appearance.

We had the opportunity to follow 7 other pa- tients with hydatid liver disease treated with al- bendozole for 9 months to 2 years. In 4 of these patients the cysts solidified into a “congealed wa-

JOURNAL OF CLINICAL ULTRASOUND

LIVER HYDATID CYST

FIGURE 2. (C) Ultrasound scan on 9 December 1986. The floating membrane is beginning to fold on itself while some of the cyst contents have solidified. (D) Ultrasound scan on 14 December 1988. The membrane is completely folded into curvilinear structures. There are no cystic elements.

VOL. 24, NO. 6, JULYiAUGUST 1996 301

SABIH ET AL.

FIGURE 2. (E) Ultrasound scan on 7 January 1992. The mass is now ill-defined and amorphous although the echogenic streaks can still be identified. (F) Ultrasound scan on 5 April 1994. The ill-defined mass remains, the streaks are visible, and the size has decreased to 4 crn.

302 JOURNAL OF CLINICAL ULTRASOUND

LIVER HYDATID CYST

terlilly” indistinguishable from the “congealed waterlilly” cyst presenting in patients who had not received medical treatment. We believed that the “congealed waterlilly” sign is reliable and strongly suggestive and allows the diagnosis of a solid hydatid to be made with confidence when recognized.

REFERENCES

1. Hadidi A: Sonography of hepatic echinococcal cysts. Gastrointest Radiol 7:349-354, 1982.

2. Weil FS: Ultrasonography of Digestive Diseases. St Louis, MO, Mosby, 1982.

3. Bolandi L, Gandolfi L, Lab0 G: Diagnostic ul- trasaound. Gastroenterology. Bologna: Piccinl Butterworth, 1984.

4. Gharbi HA, Hassine W, Brauner MW, Dupuch K: Ultrasound examination of the hydatid liver. Ra- diology 139:459-463, 1981,

5. Beggs I: The radiological appearance of hydatid disease of the liver. Clin Radiol 34:55-63, 1983.

6. Force L, Torres JM, Carrillo A, Busca J: Evalua- tion of eight serological tests in the diagnoses of human echinococcosis and follow-up. Clin Infect Dis 15473-480, 1992.

7. Gollstein B: Molecular and immunological diag- noses of echinococcosis. Clin Microbiol Rev 5:248- 261, 1992.

8. Biffin AH, Jones MA, Palmer SR: Human hydatid disease: evaluation of a n ELISA for diagnoses, pop- ulation screening and monitoring of control pro- grammes. J Med Microbiol 39:48-52, 1993.

9. Morris DL, Smith HS, Haynes A, Burrows FGO: Abdominal hydatid disease: computed tomography and ultrasound changes during albendazole ther- apy. Clin Radio1 35:297-300, 1984.

10. Lewall DB, McCorkell SJ: Rupture of echinococcal

cysts: diagnosis, classification and clinical implica- tion. A J R 146:391-394, 1986.

11. Isaacs RD: Hydatid disease, a n approach in 1986. Med Prog 25-33, 1986.

12. Barriga P, Cruz F, Lepe V, Lathoop R: An ultra- sonographically solid tumour-like appearance of echinococcal cysts in the liver. J Ultrasound Med 2:123-125, 1983.

13. Luninghans J J : In vitro grey scale echography of protein lipid fluid collection in liver tissue. J Clin Ultrasound 14:255-258, 1976.

14. Ilter T, Ozguven 0, Mentes NK: “Ball of wool” or “yarn” sign: a new ultrasonic sign for the diagnosis of hydatid cysts. A preliminary report. B J R 58:1141, 1985.

15. Garcia FJ , Marli-Bonmati L, Menor F, Rodriquez B, Ballesla A: Echogenic forms of hydatid cysts: sonographic diagnosis. J Clin Ultrasound 16:305- 311, 1988.

16. von Sinner WN: New diagnostic signs in hydatid disease; radiography, ultrasound, CT and MRI, cor- related to pathology. Eur J Radiol 12:150-159, 1991.

17. Sansot M, Le Treut Y, Burger G, et al: Semilogic des formes pseudotumorales de Kyst hydatique du foi a propos de sept. cas. Ann Radiol 26:370-375, 1983.

18. Morris DL, Dykes PW, Dickson B, Marriner SE, Bogan JA, Burrows FGO: Albendozole in hydatic disease. BMJ 286:103-104, 1983.

19. Singcharoen MD, Mahanoda N, Powell LW, Bad- deley H: Sonographic changes of hydatid cyst of the liver after treatment with mebendozole and alben- dozole. BMJ 58:905-907, 1985.

20. Filice C, Strasselli M, Brunetti E, Colombo P: U1- trasound examination of hydatid cysts treated with albendozole [letter]. J Clin Ultrasound 20~8, 569, 1992.

VOL. 24, NO. 6, JULYiAUGUST 1996 303