European Journal of Radiology, 12 ( 199 1) 150-l 59 Elsevier
150
EURRAD
00131
New diagnostic signs in hydatid disease; radiography, ultrasound, CT and MRI correlated to pathology * Walther N. von Sinner Department of Radiology, King Faisal Specialist Hospital and Research Centre. Riyadh, Saudi Arabia (Received 6 August 1990; accepted
tier
revision 16 October
Key words: Hydatid disease, Chest; Hydatid disease, Abdomen;
1990)
Radiography,
hydatid disease
Abstract Seventeen of 70 patients with hydatid disease had verified Echinococcus granulosus infection of the chest. In 14 patients (20x), the primary location was the lung parenchyma. Two patients had primary and one secondary mediastinal hydatid cysts, and one patient a primary hydatid cyst ofthe chest wall. In three above-mentioned patients, secondary pleural involvement occurred, ofwhich two were due to ruptured pulmonary cysts and one due to an hydatid cyst arising in the liver and having prolapsed into the chest. In all cases, clinical findings, radiography, ultrasound (US), computed tomography (CT) and/or magnetic resonance imaging (MRI) were correlated to macroscopic and microscopic pathology. Characteristic signs made recognition of hydatid disease possible, sometimes even when serologic tests had been non-conclusive. Assessment of other cysts throughout the body with or without involvement of neighbouring organs or tissues allowed appropriate therapeutic management. CT and MRI also played a key role in recognizing complications (e.g., rupture, infection of cysts).
Introduction Hydatid disease is a parasitic infection caused by the larval stage of the tapeworm Echinococcus. There are two main forms : the cystic unilocular form (Echinococcus granulosus) and the alveolar multilocular form (Echinococcus alveolaris) [ 10,121. Echinococcus granulosus [ l-l 1,13-421 which here is considered, is widespread throughout the world and prevalent in most sheep and cattle-raising countries. The parasite’s lifecycle requires two hosts: the definitive host is a canine (usually a dog) and the intermediate host is usually a grazing animal (sheep or cattle) or man. To avoid complications, a diagnosis should be made while the growing cyst can still be totally removed by surgery. Today, hydatid cysts can be diagnosed with the
* Presented as a scientific exhibit at the World Congress of Radiology, 1-8 July 1989 in Paris, France, where it was awarded with the Michael Katz Prize 1989. Address for reprints: Professor Walther N. von Sinner, Department of Radiology, King Faisal Specialist Hospital and Research Centre, P.O. Box 3354, Riyadh 11211, Saudi Arabia. 0720-048X/91/$03.50
0 1991 Elsevier Science Publishers
help of ultrasonography (US), computed tomography (CT) and magnetic resonance imaging (MRI). In older or damaged cysts, characteristic parasitic structures may be recognized and hydatid disease diagnosed or suspected, making serologic confirmation and appropriate diagnostic and therapeutic management feasible. US, CT and MRI also allow accurate follow-up during the post-operative and post-chemotherapeutic course of the disease. Material and Methods Over the past 10 years, 17 out of a total of 70 patients with pathologic-anatomically verified hydatid disease, have been reviewed at our institution. The ages of the patients ranged from 10 years to 67 years with an average of 30 years. There were 11 women and 6 men (with a sex relation of approximately 2 : 1). Hydatid disease in this material was localized to the chest (n = 17). Of these the lung parenchyma (n = 10) (Fig. l), the mediastinum (n = 3), the pleura (n = 3), and the chest wall (n = 1) (Fig. 3c) were infected. Clinical data, radiography, and CT were applied
B.V. (Biomedical
Division)
I
SOB
Routine CXR
Routine CXR Lt hypernephroma; CXR to exclude mets. Lt hypernephroma on CXR. ‘~metastases Cough, sputum, blood. collapsed, acute distress anaphylactic shock Liver abscess
Mass in liver
10
11
12 13
17
Note: CP. chest pain; SOB, shortness
I6
15
14
7 8 9
2 3 4 5 6
RLL LUL LUL RLL RLL Right hemithorax LLL LLL, Mediast. Pericardium
LUL
RLL + LLL
RLL + LLL
28 F
50 F
35 F
of breath; CHF, congestive
51 M
t _ _ +
+
t
_ +
+
W) (1) (M) (2) (Ml
10 cm 4 cm I :2-4 cm 2 l/2-6 cm 5 cm
5-10 cm
(M) (liver)
Calcification (liver)
(Ml
_
t
+
(Ml
3-6 cm
(1)
_
Died after op., septicemia _ _
(2)
3-8 cm
t -
+ _
(1) (M)
(1) (1)
CM)
t _
Inf.
8 cm 7 cm 6.5 cm
Rupture
t + + +
(1) (1)
Lesions
t _ + + + t
5.5 cm 6.5 cm 6 cm 7 cm 7.5 cm l-7 cm
Size
heart failure: M, multiple cysts; HC, hydatid cyst; FU, follow-up
LLL Bilat. nodules in lung. RLL + LLL
46 F 46 M
10 F
Mediastinum removal of HC (liver) LUL
15 M
21 M 17 F 43 M
F M F F F F
39 52 60 24 28 65
__~~~___
Location
~__
Age/sex
~~.._~__~_...
Atypical CP Discovered on routine CXR SOB, cough, hemoptysis Hemoptysis Atypical CP Purulent sputum. Right CP. fever, weakness Fever, purulent sputum SOB SOB. CHF
History
1
No
_
Summary of 17 patients with hydatid disease of the chest
TABLE
LU lobectomy and decortication of LLL. Mebendazole. Nil. Left nephrectomy. Mebendazole Lt rad. nephrectomy Mebendazole. LU lobectomy Decortication LLL Pleurectomy. Mebendazole. HC drained surgically; abscess. Now percutaneous drainage of HC. Evacuation of HC
Excision Mebendazole LU lobectomy RL lobectomy RL lobectomy Evacuation of cyst contents. Mebendazole Mebendazole and Albendazole FU, no growth (Mebendazole) Operated for suspected ftbr. endomyocardosis. Excision of cysts. Mebendazole.
Therapy
t
t
+
+
+ +
t
+
t t +
+ t f t + t
Pathology
152
(n = 17), and MRI was used (n = 6). CT scans were obtained with and without contrast enhancement (bolus and drip infusion, and if necessary dynamic studies), using Siemens’ Somatome DR3 (n = 17). MRI was performed with a superconductive 1.5 T scanner (Picker) using Tl- and T2-weighted conventional spinecho pulse sequences (n = 6) with the following variables: TR = 850 ms, TE = 20 ms and TR = 2000 ms, TE = 100 ms. In all patients, axial views were done. Coronal and/or sag&al views were included if further information was anticipated (n = 3). Results A summary of 17 cases of hydatid disease of the chest is given in Table 1. The history, age, sex, location, size of the lesion(s) and therapy is indicated. Several new diagnostic siglls, more or less characteristic for hydatid disease were demonstrated on US, CT and/or MRI. Two particular signs are regarded as diagnostic for hydatid cysts and were called the ‘serpent or snake sign’ (Fig. 7a-e) and the ‘spin-or whirl sign’ (Fig. 7f) representing collapsed parasitic membranes [ 401. These signs are of special interest, since they allow a confirmed diagnosis of hydatid disease. Prevalence of these signs in this material is indicated in Fig. 8. An analysis of these signs will follow with representative illustrations. Discussion Hydatid disease (Echinococcus granulosus) is prevalent both in humans and animals throughout the world and is endemic in most sheep and cattle-raising countries of the five continents. Usually, asymptomatic pulmonary hydatid disease is accidentally discovered by routine chest radiographs. Their specific diagnosis may be delayed because of (1) asymptomatic growth of the parasite during years; (2) non-specific radiographic appearance of viable nondamaged cysts; and (3) confusion with nodular lesions, primary tumors, metastases, abscesses and empyemas. The typical hydatid cyst of the lung, when discovered by chest radiography, presents as a large homogeneous nodule more than 3 cm in diameter (Fig. la). Radiographically, a ‘closed cyst’ [8,9] is often indistinguishable from other large nodular lesions, such as carcinoma of the lung, primary sarcoma of the lung, solitary metastasis, hematoma, arteriovenous aneurysm, granuloma of different etiology, abscess, infarct, inflarnmatory pseudotumor of the lung, solid or fluid-filled cysts (e.g., bronchogenic cyst, bronchiectatic cyst, dermoid cyst) and mesothelioma. If hydatid cysts grow
near compact structures (bone, chest wall, mediastinum, pleura), modification of their form, due to resistance may occur. Such lesions may be lobated, bilobated or ovoid (Fig. la). Correlations to epidemiology and pathology
Epidemiologic and pathologic-anatomic correlations are important to understand the development of clinical, radiographic, US, CT and MRI signs. A short run-down is, therefore, given. Following ingestion of eggs of the adult tapeworm, which lives in the jejunum of canines (e.g., dogs), gastroenteric enzymes digest the external coating of the eggs and the embryo is freed. The embryos migrate through the intestinal mucosa and enter the portal venules and lymphatics and from there are carried to the liver, lungs and organs and tissues supplied by the systemic circulation. Not all embryos survive; many are overcome by the host’s defence mechanisms. If the embryo is not destroyed once it has lodged in an organ, it transforms into a small cyst containing a minimal amount of fluid. Within 6 months, it grows to a small 1 cm in diameter cyst. Thereafter, it increases 2-3 cm every year, depending on the resistance of the host tissue. The host reacts against the parasite with a pericyst (adventitia). It consists of fibrous and connective tissue elements, such as collagen-containing blood vessels through which the parasite receives nutrients (Fig. lc). The parasitic cyst contains of an endocyst (germinal layer) and ectocyst (laminated membrane supporting the germinal layer). From the germinal layer brood capsules and/or daughter cysts are formed by endoproliferation. Scolices (Fig. lc) are pinched off from the germinal layer and fall to the bottom of the cyst as ‘hydatid sand’ (Fig. 5~). For years, while the cyst is growing, the patient is asymptomatic, until non-characteristic symptoms arise. According to their relative frequency, they may consist of cough, thoracic pain, expectoration, fever, hemoptysis, dyspnea, anaphylactic phenomena, vomiting and dysphagia [ 131. In older, large or damaged cysts (e.g., by trauma, toxins, infections, or chemotherapy), endogenous brood capsules (which are fixed to the germinal layer), daughter cysts and even grand-daughter cysts may develop. Less frequently, exogenous daughter cysts may originate from herniation of a portion of the cyst wall if part of the germinal layer is pinched off. If a viable hydatid cyst ruptures (Fig. lb,d) or its content is spilt (e.g., by aspiration, operation) urticaria, pyrexia and/or asthma, or anaphylactic shock, may occur. An abundance of scolices may be discharged into the peritoneum, mesenterium, lung parenchyma, pleura, liver or spleen, causing secondary hydatidosis. If a vein is
Fig. 1. A 5 l-year-old woman with left upper lobe ‘mass’. (a) Unruptured hydatid cyst in lung parenchyma; rounded, lobulated (arrows), well circumscribed and homogeneous. (b) Hazy or fuzzy contour of old pulmonary hydatid cyst. (c) Microscopic pathology: Cut through hydatid cyst wall (from inside to outside): 1, germinal layer with protoscolex; 2, hyaline membrane: 1 + 2 = parasitic cyst; and 3, pericyst or adventitia: formed by host, consisting mainly of fibroblasts containing blood vessels. (d) CT (non-enhanced): Sunburst appearance of ruptured pulmonary hydatid cyst (same as (b).
Fig. 2. A 24-year-old man withmultiple abdominalcysts: one prolapsed into chest. (a) CT without contrast enhancement (lower chest): prolapsed hydatid cyst (arrow). (b) MRI (T2-weighted; SE 2000/100): prolapsed hydatid cyst containing low intensity rim (small black arrows), high density contents with daughter cyst (large black arrow), and halo due to reactive or compressed lung parenchyma (white arrows). (c) Microscopic pathology: parasitic membranes with bile pigment from old bilio-cystic listula, confirming that this cyst had originated in the liver and prolapsed into the chest.
eroded and viable cystic content is discharged metastatic hydatidosis ensues. Primary hydatid cysts may occur in any organ or tissue. Multiple cysts in the same or in different organs may coexist or develop successively. The frequency of hydatid cysts in the literature is the following: liver 60-75 %, lung 15-25 % and remaining parts of the body 10-15x [l-39]. This corresponds well with the assumption that 25-35 y0 of the embryos pass the liver filter, and 10-15x the pulmonary filter reaching the systemic circulation. The lung can also be reached by (1) venules and lymph vessels bypassing the liver; (2) by the lymph vessels from the abdomen via the thoracic duct and the left subclavian vein to the superior vena cava. Expanding cysts sooner or later reach a bronchiolus;
after its erosion, a communication is established between the enveloping adventitia or pericyst (provided by the host), and the bronchial tree (‘communicating cyst’). This causes a variety of more or less characteristic radiographic signs, which may raise suspicion about the presence of hydatid cyst(s) or even allow a specific diagnosis of hydatid disease [8,9] (Fig. 7a). Radiographic signs Echinococcosis has captured the imagination of early researchers to such a degree that they gave ‘fancy’ names to these radiographic signs. Only the most important can here be mentioned. If air (e.g., with coughing or spontaneously) penetrates into the virtual space between the adventitia (pericyst) and ectocyst (laminated membrane of the parasite), local detachment
Fig. 3. Brood capsule and daughter cyst sign: (a) Ultrasound: multiple daughter cysts in an abdominal hydatid cyst. (b) CT of liver: hydatid cyst; multiple daughter cysts and brood capsules (connected to germinal layer); endogenous proliferation. (c) MRI (SE 2000/100): Hydatid cyst of right chest wall, sag&al cut; multiple daughter cysts (arrows); exogenous and endogenous proliferation. Low-density rim (arrow heads).
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of parasitic membranes from the pericyst, called the ‘sign of detachment’ develops. This segmental peripheral radiolucency, called the ‘crescent’ or the ‘meniscus sign’ may also occur with cavities containing a fungus ball, blood clot, chunk of tumor (such as in cavitating squamous cell carcinoma) and some other tumors (e.g., hamartoma, bronchial adenoma), and is therefore not specific for hydatid disease. If more air is introduced the parasitic membranes (endocyst) collapse further, and an air-fluid level is seen. If the parasitic membranes are floating on the fluid surface, like leaves of a water lily, a ‘water-lily sign’ or ‘camalote sign’ is present. Calcifications of cysts in the liver and abdomen, and even in the rest of the body, are not uncommon. However, in the lung parenchyma, they are extremely rare. They have been called ‘egg-shell calcification’ if the whole cyst wall is calcified, ‘crushed egg calcification’ if the wall is compressed and fractured, or ‘sunburst calcification’ if processes are flaring out. These signs usually indicate that the cyst is already dead. Partial calcifications of the cyst wall, however, may still co-exist with a viable parasite. Small or minute calcium deposits in the pericyst and rarely in parasitic membranes or daughter cysts are best seen with non-enhanced CT.
Fig. 4. Rim sign: MRI: Low-density
Ultrasonographic, CT and MRI signs
To the preceding well known signs, I wish to add some signs which not only have a specific pathologicanatomic basis, but also on US, CT and/or MRI demonstrate a characteristic pattern. In some cases, they may only raise suspicion about the presence of hydatid disease; with one or more characteristic signs, a confirmed diagnosis of echinococcosis may be possible. Daughter cyst sign
On conventional radiographs, brood capsules and/or daughter cysts are only seen if they are calcified [ 121. In the liver and other abdominal locations, daughter cysts can easily be identified with ultrasound [3,9], (Fig. 3a), CT [ lS,lS] (Fig. 3b) or MRI (Figs. 2b and 3~). ‘Hydatid sand’ (Fig. 5c) and daughter cysts (Fig. 3a,b,c) are characteristic for hydatid disease. Free daughter cysts may move according to gravity with different positions of the patient’s body. On MRI, daughter cysts may demonstrate a high- or low-signal intensity [ 171, depending on their contents (composition or absorption of fluid, infection, degeneration of parasitic material and scolices). If brood capsules or daughter cysts are regularly formed in the periphery of the cyst wall around the
rim of hydatid cyst (arrows). (a) TZ-weighted (SE 2000/100). (b) Tl-weighted
(SE 850/20).
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Fig. 5. Cyst WIN sign: (a) CT without contrast enhancement: large liver cyst. (b) Ultrasound: ethos at bottom of cyst: hydatid sand (arrows). Multiple cysts with septum sign: (c) CT without contrast enhancement: multiple septated cysts (white arrows); some show edema (black arrows) surrounding the cyst after albendazole treatment.
cystic circumference, a ‘cartwheel appearance’ arises. Free daughter cysts have the appearance of a ‘cyst (or cysts) within a cyst’ (Fig. 3a,b,c). Rim sign On MRI the presence of a low-signal intensity rim separating the parasitic cyst from the patient’s tissue assumed to represent the pericyst has already been observed in liver cysts [ 16-201. Recently, I have observed this low-intensity rim not only in liver (Fig. 7d,e,f), brain [43] and bone cysts but also in pulmonary hydatid cysts [36,37,40] where it seems to be even more conspicuous if it is contiguous to the thoracic
wall (Figs. 2b and 3c) and less conspicuous if it is bordering lung parenchyma [ 171. This latter phenomenon is probably due to lack of contrast between lung parenchyma and the cyst (Fig. Id). Serpent sign Collapse of parasitic membranes occurs secondary to damage or degeneration of hydatid cysts with rupture of the endocyst and may be recognized by ultrasonography, CT and MRI. On Tl- and T2-weighted MR images it has not been described until recently. It is an important diagnostic sign for the diagnosis of hydatid disease (Fig. 7). Because of the ‘snake’ appearance on
Fig. 6. Air bubble sign and ring enhancement: (a) CT (without contrast enhancement) air bubbles within lesion (arrows). (b) CT (dynamic study): demonstrating ring enhancement of pericyst (arrowheads). Perforated cyst wall with paracystic emphysema (curved arrows) and air bubbles (small arrows) within cyst.
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ultrasound, CT and MRI, I have called this sign ‘serpent or snake sign’ [40] (Fig. 7b,c,d and e). It is only rarely seen with conventional radiography (Fig. 7a). On ultrasound, ‘parallel stripes’ [40-421 represent contact of the parasite’s ectocyst with the host’s pericyst. If parasitic membranes collapse, the double line disappears and a ‘serpent or snake sign’ develops. Spin or whirl sign Collapsed parasitic membranes on MRI may present with a gyrated and bosseled appearance (Fig. 7f). This is another diagnostic sign of a hydatid cyst. It may occur with outer rupture of the cyst wall demonstrating spillage of cyst content through a defective low-intensity rim (Fig. 7f). Because of the twirled and twisted appearance of the collapsed parasitic membrane I called it ‘spin-or whirl sign’; like the serpent sign, it is important because it is strong evidence for the diagnosis of hydatid
disease even if serologic tests should be unavailable falsely negative.
or
Air bubble sign Most ruptured cysts become infected. Air may enter the cyst by dissection of (a) pericyst and parasitic membranes; (b) with the erosion of a bronchiolus causing a bronchiolar-cystic fistula; or (c) by communication with an air-containing organ or duct (e.g., bile duct), and (d) possibly by gas-generating bacteria. Retained parasitic material in a hydatid cyst is particularly prone for infection and abscess formation. Air bubbles may be identified on chest radiographs, linear tomographs, ultrasonography, CT (Figs. 2a, 6a and b) and MRI. Cyst wall sign The wall of a hydatid cyst can be visualized by ultrasonography (Figs. 3a and 7b), CT (Figs. 3b and 5a) and
sign’ (collapsed parasitic membranes) and ‘halo sign’: Pulmonary cyst: (a) Radiograph, ‘serpent or snake sign’ (arrows). Hepatic Serpent or snake sign of hepatic hydatid cyst (arrow). (c) CT: serpent or snake sign in hepatic hydatid cyst (arrows). (d) MRI (T2-weighted; SE 2000/100): Serpent or snake sign (black arrows) with halo (large white arrows). Pericyst (small white arrows). (e) MRI (Tl-weighted; SE 850/20): Serpent or snake sign (white small arrows). Pericyst (small black arrows). Halo due to edema (large white arrows). (f) MRI (T2-weighted; SE 2000/100): ‘spin or whirl sign’. See also rupture of low-intensity rim (black arrows) with spillage of cyst content (curved black arrows) and halo due to reaction (curved white arrows) of surrounding liver tissue (edema). Fig. 7. Serpent
cyst: (b) Ultrasound:
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MRI (Figs. 2b, 4a and b). If several embryos are embolized close together, they may first develop as individual cysts. With expanding growth, the wall of these cysts touch each other and affect the form of the cysts by mutual compression. Hydatid cysts seldom fuse into a single cyst; often the cystic wall is preserved, although stretching and deformation occurs, making the impression ofbranching septations (e.g., ‘Y-form’ or ‘mercedes star’ forms) (Fig. 5b). Ring enhancement
12-r
lo-
8-
6-
sign
Due to vascularization of the pericyst (Fig. lc), there may be ring enhancement secondary to contrast application. This occurs mainly in infected hydatid cysts due to hypervascularization of the adventitial layer (pericyst). With angiography, a ring-like blush may be seen. With CT and MRI, ring enhancement not unlike an abscess is noted, with which it may be confused (Fig. 6b). Halo sign
In pulmonary hydatid cysts, in addition to the ring enhancement sign a dense halo may be seen on CT and MRI surrounding the cyst, caused by allergic orinflammatory infiltrates or atelectatic lung (Fig. 2b). A halo may also be! seen in abdominal cysts (e.g., in the liver) caused by edema, necrosis or inflammatory reaction of the surrounding liver tissue (e.g., secondary to albendazole treatment) and, therefore, indicates a degenerated or damaged hydatid cyst (Fig. 7d,e and I). Sunburst sign
Old, damaged, or ruptured cysts may display a These changes have been ‘sunburst appearance’. described on chest radiographs [l-4,22] (Fig. lb), and may also be demonstrated on CT (Fig. Id) and MRI. Pseudocyst sign
Post-surgical cysts may resemble recurrent hydatid cysts [39]. According to the surgical procedure used, different Hounsfield units ( - 100 to 35 HU) may be found depending if mesenterial fat has been used or not to fill the cavity caused by excision of the cyst. Additional signs consist of a flattened form of the cyst and an increased thickness of the cystic walls. Pre- and post-operative CT-findings are important for comparison and evaluation of possible pseudocysts. Conclusions (1) Hydatid disease may present with a variety of patterns (Fig. 8). Closed cysts cannot be recognized as hydatid cysts by radiographs alone unless other cysts
0
1 2
3 4 5 6 7 8 91011121314151617181920
Fig. 8. Signs and symptoms: symptoms in 17 patients with hydatid disease of the chest.
(e.g., calcifications in liver in 16%) elsewhere are discovered or serological tests are performed and prove positive for echinococcus. (2) Ultrasonography identifies ‘nodules’ as cysts but is not always diagnostically conclusive in closed cysts except with the presence of ‘parallel stripes’. It may, however, be helpful in raising suspicion about the presence of hydatid disease; it is more often diagnostic in complicated hydatid cysts. (3) CT and MRI may identify large ‘nodules’ as hydatid cysts in demonstrating characteristic signs both in closed and ruptured cysts. (4) Several new diagnostic signs (‘serpent or snake sign’ and ‘spin or whirl sign’) are helpful in a confident and or specific diagnosis of hydatid disease; sometimes even if serology should be falsely negative or pathologic proof is lacking. (5) Complications (such as rupture, infection, dissemination of hydatid cysts, reaction of neighboring parenchyma or pleura) may be recognized. (6) Hydatid cysts with other localization than the chest can be identified and assessed. (7) Pleural, abdominal and pelvic dissemination as a complication secondary to rupture of HD can be recognized and evaluated. (8) New effective chemotherapeutic agents (e.g., albendazole) have recently become feasible and may improve the long-term prognosis of disseminated nonoperable hydatid disease. The effect of therapy can be monitored and followed by US, CT and MRI, and
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recurrence may be detected been done.
before much damage has 18 19
Acknowledgements I thank Dr. A. Ali, Department of Pathology, King Faisal Specialist Hospital and Research Center, Riyadh, for pathologic workup of the specimen, the photographic department for help with illustrations, and Miss Catherine Devane and Miss Catherine Healy for their skilful secretarial assistance.
20 21 22
23 24
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EURRAD
00131
New diagnostic signs in hydatid disease; radiography, ultrasound, CT and MRI correlated to pathology * Walther N. von Sinner Department of Radiology, King Faisal Specialist Hospital and Research Centre. Riyadh, Saudi Arabia (Received 6 August 1990; accepted
tier
revision 16 October
Key words: Hydatid disease, Chest; Hydatid disease, Abdomen;
1990)
Radiography,
hydatid disease
Abstract Seventeen of 70 patients with hydatid disease had verified Echinococcus granulosus infection of the chest. In 14 patients (20x), the primary location was the lung parenchyma. Two patients had primary and one secondary mediastinal hydatid cysts, and one patient a primary hydatid cyst ofthe chest wall. In three above-mentioned patients, secondary pleural involvement occurred, ofwhich two were due to ruptured pulmonary cysts and one due to an hydatid cyst arising in the liver and having prolapsed into the chest. In all cases, clinical findings, radiography, ultrasound (US), computed tomography (CT) and/or magnetic resonance imaging (MRI) were correlated to macroscopic and microscopic pathology. Characteristic signs made recognition of hydatid disease possible, sometimes even when serologic tests had been non-conclusive. Assessment of other cysts throughout the body with or without involvement of neighbouring organs or tissues allowed appropriate therapeutic management. CT and MRI also played a key role in recognizing complications (e.g., rupture, infection of cysts).
Introduction Hydatid disease is a parasitic infection caused by the larval stage of the tapeworm Echinococcus. There are two main forms : the cystic unilocular form (Echinococcus granulosus) and the alveolar multilocular form (Echinococcus alveolaris) [ 10,121. Echinococcus granulosus [ l-l 1,13-421 which here is considered, is widespread throughout the world and prevalent in most sheep and cattle-raising countries. The parasite’s lifecycle requires two hosts: the definitive host is a canine (usually a dog) and the intermediate host is usually a grazing animal (sheep or cattle) or man. To avoid complications, a diagnosis should be made while the growing cyst can still be totally removed by surgery. Today, hydatid cysts can be diagnosed with the
* Presented as a scientific exhibit at the World Congress of Radiology, 1-8 July 1989 in Paris, France, where it was awarded with the Michael Katz Prize 1989. Address for reprints: Professor Walther N. von Sinner, Department of Radiology, King Faisal Specialist Hospital and Research Centre, P.O. Box 3354, Riyadh 11211, Saudi Arabia. 0720-048X/91/$03.50
0 1991 Elsevier Science Publishers
help of ultrasonography (US), computed tomography (CT) and magnetic resonance imaging (MRI). In older or damaged cysts, characteristic parasitic structures may be recognized and hydatid disease diagnosed or suspected, making serologic confirmation and appropriate diagnostic and therapeutic management feasible. US, CT and MRI also allow accurate follow-up during the post-operative and post-chemotherapeutic course of the disease. Material and Methods Over the past 10 years, 17 out of a total of 70 patients with pathologic-anatomically verified hydatid disease, have been reviewed at our institution. The ages of the patients ranged from 10 years to 67 years with an average of 30 years. There were 11 women and 6 men (with a sex relation of approximately 2 : 1). Hydatid disease in this material was localized to the chest (n = 17). Of these the lung parenchyma (n = 10) (Fig. l), the mediastinum (n = 3), the pleura (n = 3), and the chest wall (n = 1) (Fig. 3c) were infected. Clinical data, radiography, and CT were applied
B.V. (Biomedical
Division)
I
SOB
Routine CXR
Routine CXR Lt hypernephroma; CXR to exclude mets. Lt hypernephroma on CXR. ‘~metastases Cough, sputum, blood. collapsed, acute distress anaphylactic shock Liver abscess
Mass in liver
10
11
12 13
17
Note: CP. chest pain; SOB, shortness
I6
15
14
7 8 9
2 3 4 5 6
RLL LUL LUL RLL RLL Right hemithorax LLL LLL, Mediast. Pericardium
LUL
RLL + LLL
RLL + LLL
28 F
50 F
35 F
of breath; CHF, congestive
51 M
t _ _ +
+
t
_ +
+
W) (1) (M) (2) (Ml
10 cm 4 cm I :2-4 cm 2 l/2-6 cm 5 cm
5-10 cm
(M) (liver)
Calcification (liver)
(Ml
_
t
+
(Ml
3-6 cm
(1)
_
Died after op., septicemia _ _
(2)
3-8 cm
t -
+ _
(1) (M)
(1) (1)
CM)
t _
Inf.
8 cm 7 cm 6.5 cm
Rupture
t + + +
(1) (1)
Lesions
t _ + + + t
5.5 cm 6.5 cm 6 cm 7 cm 7.5 cm l-7 cm
Size
heart failure: M, multiple cysts; HC, hydatid cyst; FU, follow-up
LLL Bilat. nodules in lung. RLL + LLL
46 F 46 M
10 F
Mediastinum removal of HC (liver) LUL
15 M
21 M 17 F 43 M
F M F F F F
39 52 60 24 28 65
__~~~___
Location
~__
Age/sex
~~.._~__~_...
Atypical CP Discovered on routine CXR SOB, cough, hemoptysis Hemoptysis Atypical CP Purulent sputum. Right CP. fever, weakness Fever, purulent sputum SOB SOB. CHF
History
1
No
_
Summary of 17 patients with hydatid disease of the chest
TABLE
LU lobectomy and decortication of LLL. Mebendazole. Nil. Left nephrectomy. Mebendazole Lt rad. nephrectomy Mebendazole. LU lobectomy Decortication LLL Pleurectomy. Mebendazole. HC drained surgically; abscess. Now percutaneous drainage of HC. Evacuation of HC
Excision Mebendazole LU lobectomy RL lobectomy RL lobectomy Evacuation of cyst contents. Mebendazole Mebendazole and Albendazole FU, no growth (Mebendazole) Operated for suspected ftbr. endomyocardosis. Excision of cysts. Mebendazole.
Therapy
t
t
+
+
+ +
t
+
t t +
+ t f t + t
Pathology
152
(n = 17), and MRI was used (n = 6). CT scans were obtained with and without contrast enhancement (bolus and drip infusion, and if necessary dynamic studies), using Siemens’ Somatome DR3 (n = 17). MRI was performed with a superconductive 1.5 T scanner (Picker) using Tl- and T2-weighted conventional spinecho pulse sequences (n = 6) with the following variables: TR = 850 ms, TE = 20 ms and TR = 2000 ms, TE = 100 ms. In all patients, axial views were done. Coronal and/or sag&al views were included if further information was anticipated (n = 3). Results A summary of 17 cases of hydatid disease of the chest is given in Table 1. The history, age, sex, location, size of the lesion(s) and therapy is indicated. Several new diagnostic siglls, more or less characteristic for hydatid disease were demonstrated on US, CT and/or MRI. Two particular signs are regarded as diagnostic for hydatid cysts and were called the ‘serpent or snake sign’ (Fig. 7a-e) and the ‘spin-or whirl sign’ (Fig. 7f) representing collapsed parasitic membranes [ 401. These signs are of special interest, since they allow a confirmed diagnosis of hydatid disease. Prevalence of these signs in this material is indicated in Fig. 8. An analysis of these signs will follow with representative illustrations. Discussion Hydatid disease (Echinococcus granulosus) is prevalent both in humans and animals throughout the world and is endemic in most sheep and cattle-raising countries of the five continents. Usually, asymptomatic pulmonary hydatid disease is accidentally discovered by routine chest radiographs. Their specific diagnosis may be delayed because of (1) asymptomatic growth of the parasite during years; (2) non-specific radiographic appearance of viable nondamaged cysts; and (3) confusion with nodular lesions, primary tumors, metastases, abscesses and empyemas. The typical hydatid cyst of the lung, when discovered by chest radiography, presents as a large homogeneous nodule more than 3 cm in diameter (Fig. la). Radiographically, a ‘closed cyst’ [8,9] is often indistinguishable from other large nodular lesions, such as carcinoma of the lung, primary sarcoma of the lung, solitary metastasis, hematoma, arteriovenous aneurysm, granuloma of different etiology, abscess, infarct, inflarnmatory pseudotumor of the lung, solid or fluid-filled cysts (e.g., bronchogenic cyst, bronchiectatic cyst, dermoid cyst) and mesothelioma. If hydatid cysts grow
near compact structures (bone, chest wall, mediastinum, pleura), modification of their form, due to resistance may occur. Such lesions may be lobated, bilobated or ovoid (Fig. la). Correlations to epidemiology and pathology
Epidemiologic and pathologic-anatomic correlations are important to understand the development of clinical, radiographic, US, CT and MRI signs. A short run-down is, therefore, given. Following ingestion of eggs of the adult tapeworm, which lives in the jejunum of canines (e.g., dogs), gastroenteric enzymes digest the external coating of the eggs and the embryo is freed. The embryos migrate through the intestinal mucosa and enter the portal venules and lymphatics and from there are carried to the liver, lungs and organs and tissues supplied by the systemic circulation. Not all embryos survive; many are overcome by the host’s defence mechanisms. If the embryo is not destroyed once it has lodged in an organ, it transforms into a small cyst containing a minimal amount of fluid. Within 6 months, it grows to a small 1 cm in diameter cyst. Thereafter, it increases 2-3 cm every year, depending on the resistance of the host tissue. The host reacts against the parasite with a pericyst (adventitia). It consists of fibrous and connective tissue elements, such as collagen-containing blood vessels through which the parasite receives nutrients (Fig. lc). The parasitic cyst contains of an endocyst (germinal layer) and ectocyst (laminated membrane supporting the germinal layer). From the germinal layer brood capsules and/or daughter cysts are formed by endoproliferation. Scolices (Fig. lc) are pinched off from the germinal layer and fall to the bottom of the cyst as ‘hydatid sand’ (Fig. 5~). For years, while the cyst is growing, the patient is asymptomatic, until non-characteristic symptoms arise. According to their relative frequency, they may consist of cough, thoracic pain, expectoration, fever, hemoptysis, dyspnea, anaphylactic phenomena, vomiting and dysphagia [ 131. In older, large or damaged cysts (e.g., by trauma, toxins, infections, or chemotherapy), endogenous brood capsules (which are fixed to the germinal layer), daughter cysts and even grand-daughter cysts may develop. Less frequently, exogenous daughter cysts may originate from herniation of a portion of the cyst wall if part of the germinal layer is pinched off. If a viable hydatid cyst ruptures (Fig. lb,d) or its content is spilt (e.g., by aspiration, operation) urticaria, pyrexia and/or asthma, or anaphylactic shock, may occur. An abundance of scolices may be discharged into the peritoneum, mesenterium, lung parenchyma, pleura, liver or spleen, causing secondary hydatidosis. If a vein is
Fig. 1. A 5 l-year-old woman with left upper lobe ‘mass’. (a) Unruptured hydatid cyst in lung parenchyma; rounded, lobulated (arrows), well circumscribed and homogeneous. (b) Hazy or fuzzy contour of old pulmonary hydatid cyst. (c) Microscopic pathology: Cut through hydatid cyst wall (from inside to outside): 1, germinal layer with protoscolex; 2, hyaline membrane: 1 + 2 = parasitic cyst; and 3, pericyst or adventitia: formed by host, consisting mainly of fibroblasts containing blood vessels. (d) CT (non-enhanced): Sunburst appearance of ruptured pulmonary hydatid cyst (same as (b).
Fig. 2. A 24-year-old man withmultiple abdominalcysts: one prolapsed into chest. (a) CT without contrast enhancement (lower chest): prolapsed hydatid cyst (arrow). (b) MRI (T2-weighted; SE 2000/100): prolapsed hydatid cyst containing low intensity rim (small black arrows), high density contents with daughter cyst (large black arrow), and halo due to reactive or compressed lung parenchyma (white arrows). (c) Microscopic pathology: parasitic membranes with bile pigment from old bilio-cystic listula, confirming that this cyst had originated in the liver and prolapsed into the chest.
eroded and viable cystic content is discharged metastatic hydatidosis ensues. Primary hydatid cysts may occur in any organ or tissue. Multiple cysts in the same or in different organs may coexist or develop successively. The frequency of hydatid cysts in the literature is the following: liver 60-75 %, lung 15-25 % and remaining parts of the body 10-15x [l-39]. This corresponds well with the assumption that 25-35 y0 of the embryos pass the liver filter, and 10-15x the pulmonary filter reaching the systemic circulation. The lung can also be reached by (1) venules and lymph vessels bypassing the liver; (2) by the lymph vessels from the abdomen via the thoracic duct and the left subclavian vein to the superior vena cava. Expanding cysts sooner or later reach a bronchiolus;
after its erosion, a communication is established between the enveloping adventitia or pericyst (provided by the host), and the bronchial tree (‘communicating cyst’). This causes a variety of more or less characteristic radiographic signs, which may raise suspicion about the presence of hydatid cyst(s) or even allow a specific diagnosis of hydatid disease [8,9] (Fig. 7a). Radiographic signs Echinococcosis has captured the imagination of early researchers to such a degree that they gave ‘fancy’ names to these radiographic signs. Only the most important can here be mentioned. If air (e.g., with coughing or spontaneously) penetrates into the virtual space between the adventitia (pericyst) and ectocyst (laminated membrane of the parasite), local detachment
Fig. 3. Brood capsule and daughter cyst sign: (a) Ultrasound: multiple daughter cysts in an abdominal hydatid cyst. (b) CT of liver: hydatid cyst; multiple daughter cysts and brood capsules (connected to germinal layer); endogenous proliferation. (c) MRI (SE 2000/100): Hydatid cyst of right chest wall, sag&al cut; multiple daughter cysts (arrows); exogenous and endogenous proliferation. Low-density rim (arrow heads).
155
of parasitic membranes from the pericyst, called the ‘sign of detachment’ develops. This segmental peripheral radiolucency, called the ‘crescent’ or the ‘meniscus sign’ may also occur with cavities containing a fungus ball, blood clot, chunk of tumor (such as in cavitating squamous cell carcinoma) and some other tumors (e.g., hamartoma, bronchial adenoma), and is therefore not specific for hydatid disease. If more air is introduced the parasitic membranes (endocyst) collapse further, and an air-fluid level is seen. If the parasitic membranes are floating on the fluid surface, like leaves of a water lily, a ‘water-lily sign’ or ‘camalote sign’ is present. Calcifications of cysts in the liver and abdomen, and even in the rest of the body, are not uncommon. However, in the lung parenchyma, they are extremely rare. They have been called ‘egg-shell calcification’ if the whole cyst wall is calcified, ‘crushed egg calcification’ if the wall is compressed and fractured, or ‘sunburst calcification’ if processes are flaring out. These signs usually indicate that the cyst is already dead. Partial calcifications of the cyst wall, however, may still co-exist with a viable parasite. Small or minute calcium deposits in the pericyst and rarely in parasitic membranes or daughter cysts are best seen with non-enhanced CT.
Fig. 4. Rim sign: MRI: Low-density
Ultrasonographic, CT and MRI signs
To the preceding well known signs, I wish to add some signs which not only have a specific pathologicanatomic basis, but also on US, CT and/or MRI demonstrate a characteristic pattern. In some cases, they may only raise suspicion about the presence of hydatid disease; with one or more characteristic signs, a confirmed diagnosis of echinococcosis may be possible. Daughter cyst sign
On conventional radiographs, brood capsules and/or daughter cysts are only seen if they are calcified [ 121. In the liver and other abdominal locations, daughter cysts can easily be identified with ultrasound [3,9], (Fig. 3a), CT [ lS,lS] (Fig. 3b) or MRI (Figs. 2b and 3~). ‘Hydatid sand’ (Fig. 5c) and daughter cysts (Fig. 3a,b,c) are characteristic for hydatid disease. Free daughter cysts may move according to gravity with different positions of the patient’s body. On MRI, daughter cysts may demonstrate a high- or low-signal intensity [ 171, depending on their contents (composition or absorption of fluid, infection, degeneration of parasitic material and scolices). If brood capsules or daughter cysts are regularly formed in the periphery of the cyst wall around the
rim of hydatid cyst (arrows). (a) TZ-weighted (SE 2000/100). (b) Tl-weighted
(SE 850/20).
156
Fig. 5. Cyst WIN sign: (a) CT without contrast enhancement: large liver cyst. (b) Ultrasound: ethos at bottom of cyst: hydatid sand (arrows). Multiple cysts with septum sign: (c) CT without contrast enhancement: multiple septated cysts (white arrows); some show edema (black arrows) surrounding the cyst after albendazole treatment.
cystic circumference, a ‘cartwheel appearance’ arises. Free daughter cysts have the appearance of a ‘cyst (or cysts) within a cyst’ (Fig. 3a,b,c). Rim sign On MRI the presence of a low-signal intensity rim separating the parasitic cyst from the patient’s tissue assumed to represent the pericyst has already been observed in liver cysts [ 16-201. Recently, I have observed this low-intensity rim not only in liver (Fig. 7d,e,f), brain [43] and bone cysts but also in pulmonary hydatid cysts [36,37,40] where it seems to be even more conspicuous if it is contiguous to the thoracic
wall (Figs. 2b and 3c) and less conspicuous if it is bordering lung parenchyma [ 171. This latter phenomenon is probably due to lack of contrast between lung parenchyma and the cyst (Fig. Id). Serpent sign Collapse of parasitic membranes occurs secondary to damage or degeneration of hydatid cysts with rupture of the endocyst and may be recognized by ultrasonography, CT and MRI. On Tl- and T2-weighted MR images it has not been described until recently. It is an important diagnostic sign for the diagnosis of hydatid disease (Fig. 7). Because of the ‘snake’ appearance on
Fig. 6. Air bubble sign and ring enhancement: (a) CT (without contrast enhancement) air bubbles within lesion (arrows). (b) CT (dynamic study): demonstrating ring enhancement of pericyst (arrowheads). Perforated cyst wall with paracystic emphysema (curved arrows) and air bubbles (small arrows) within cyst.
157
ultrasound, CT and MRI, I have called this sign ‘serpent or snake sign’ [40] (Fig. 7b,c,d and e). It is only rarely seen with conventional radiography (Fig. 7a). On ultrasound, ‘parallel stripes’ [40-421 represent contact of the parasite’s ectocyst with the host’s pericyst. If parasitic membranes collapse, the double line disappears and a ‘serpent or snake sign’ develops. Spin or whirl sign Collapsed parasitic membranes on MRI may present with a gyrated and bosseled appearance (Fig. 7f). This is another diagnostic sign of a hydatid cyst. It may occur with outer rupture of the cyst wall demonstrating spillage of cyst content through a defective low-intensity rim (Fig. 7f). Because of the twirled and twisted appearance of the collapsed parasitic membrane I called it ‘spin-or whirl sign’; like the serpent sign, it is important because it is strong evidence for the diagnosis of hydatid
disease even if serologic tests should be unavailable falsely negative.
or
Air bubble sign Most ruptured cysts become infected. Air may enter the cyst by dissection of (a) pericyst and parasitic membranes; (b) with the erosion of a bronchiolus causing a bronchiolar-cystic fistula; or (c) by communication with an air-containing organ or duct (e.g., bile duct), and (d) possibly by gas-generating bacteria. Retained parasitic material in a hydatid cyst is particularly prone for infection and abscess formation. Air bubbles may be identified on chest radiographs, linear tomographs, ultrasonography, CT (Figs. 2a, 6a and b) and MRI. Cyst wall sign The wall of a hydatid cyst can be visualized by ultrasonography (Figs. 3a and 7b), CT (Figs. 3b and 5a) and
sign’ (collapsed parasitic membranes) and ‘halo sign’: Pulmonary cyst: (a) Radiograph, ‘serpent or snake sign’ (arrows). Hepatic Serpent or snake sign of hepatic hydatid cyst (arrow). (c) CT: serpent or snake sign in hepatic hydatid cyst (arrows). (d) MRI (T2-weighted; SE 2000/100): Serpent or snake sign (black arrows) with halo (large white arrows). Pericyst (small white arrows). (e) MRI (Tl-weighted; SE 850/20): Serpent or snake sign (white small arrows). Pericyst (small black arrows). Halo due to edema (large white arrows). (f) MRI (T2-weighted; SE 2000/100): ‘spin or whirl sign’. See also rupture of low-intensity rim (black arrows) with spillage of cyst content (curved black arrows) and halo due to reaction (curved white arrows) of surrounding liver tissue (edema). Fig. 7. Serpent
cyst: (b) Ultrasound:
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MRI (Figs. 2b, 4a and b). If several embryos are embolized close together, they may first develop as individual cysts. With expanding growth, the wall of these cysts touch each other and affect the form of the cysts by mutual compression. Hydatid cysts seldom fuse into a single cyst; often the cystic wall is preserved, although stretching and deformation occurs, making the impression ofbranching septations (e.g., ‘Y-form’ or ‘mercedes star’ forms) (Fig. 5b). Ring enhancement
12-r
lo-
8-
6-
sign
Due to vascularization of the pericyst (Fig. lc), there may be ring enhancement secondary to contrast application. This occurs mainly in infected hydatid cysts due to hypervascularization of the adventitial layer (pericyst). With angiography, a ring-like blush may be seen. With CT and MRI, ring enhancement not unlike an abscess is noted, with which it may be confused (Fig. 6b). Halo sign
In pulmonary hydatid cysts, in addition to the ring enhancement sign a dense halo may be seen on CT and MRI surrounding the cyst, caused by allergic orinflammatory infiltrates or atelectatic lung (Fig. 2b). A halo may also be! seen in abdominal cysts (e.g., in the liver) caused by edema, necrosis or inflammatory reaction of the surrounding liver tissue (e.g., secondary to albendazole treatment) and, therefore, indicates a degenerated or damaged hydatid cyst (Fig. 7d,e and I). Sunburst sign
Old, damaged, or ruptured cysts may display a These changes have been ‘sunburst appearance’. described on chest radiographs [l-4,22] (Fig. lb), and may also be demonstrated on CT (Fig. Id) and MRI. Pseudocyst sign
Post-surgical cysts may resemble recurrent hydatid cysts [39]. According to the surgical procedure used, different Hounsfield units ( - 100 to 35 HU) may be found depending if mesenterial fat has been used or not to fill the cavity caused by excision of the cyst. Additional signs consist of a flattened form of the cyst and an increased thickness of the cystic walls. Pre- and post-operative CT-findings are important for comparison and evaluation of possible pseudocysts. Conclusions (1) Hydatid disease may present with a variety of patterns (Fig. 8). Closed cysts cannot be recognized as hydatid cysts by radiographs alone unless other cysts
0
1 2
3 4 5 6 7 8 91011121314151617181920
Fig. 8. Signs and symptoms: symptoms in 17 patients with hydatid disease of the chest.
(e.g., calcifications in liver in 16%) elsewhere are discovered or serological tests are performed and prove positive for echinococcus. (2) Ultrasonography identifies ‘nodules’ as cysts but is not always diagnostically conclusive in closed cysts except with the presence of ‘parallel stripes’. It may, however, be helpful in raising suspicion about the presence of hydatid disease; it is more often diagnostic in complicated hydatid cysts. (3) CT and MRI may identify large ‘nodules’ as hydatid cysts in demonstrating characteristic signs both in closed and ruptured cysts. (4) Several new diagnostic signs (‘serpent or snake sign’ and ‘spin or whirl sign’) are helpful in a confident and or specific diagnosis of hydatid disease; sometimes even if serology should be falsely negative or pathologic proof is lacking. (5) Complications (such as rupture, infection, dissemination of hydatid cysts, reaction of neighboring parenchyma or pleura) may be recognized. (6) Hydatid cysts with other localization than the chest can be identified and assessed. (7) Pleural, abdominal and pelvic dissemination as a complication secondary to rupture of HD can be recognized and evaluated. (8) New effective chemotherapeutic agents (e.g., albendazole) have recently become feasible and may improve the long-term prognosis of disseminated nonoperable hydatid disease. The effect of therapy can be monitored and followed by US, CT and MRI, and
159
recurrence may be detected been done.
before much damage has 18 19
Acknowledgements I thank Dr. A. Ali, Department of Pathology, King Faisal Specialist Hospital and Research Center, Riyadh, for pathologic workup of the specimen, the photographic department for help with illustrations, and Miss Catherine Devane and Miss Catherine Healy for their skilful secretarial assistance.
20 21 22
23 24
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