Hydatid disease: Biology, pathology, imaging and classification

Clinical Radiology (1998) 53, 863-874

Review Hydatid Disease:Biology, Pathology, Imaging and Classification D. B. LEWALL

Department of Medical Imaging, King Fahad National Guard Hospital, Riyadh, Kingdom of Saudi Arabia

Rupture and the sequellae of rupture are more important than the mass effect of hydatid cysts, except in the brain where the mass effect by itself has severe consequences. The biology of hydatid disease, including the complex interaction between primary and secondary hosts, is reviewed. The hydatid cyst always starts as a fluid-filled, cyst-like structure (Type I) which may proceed to a Type II lesion if daughter cysts and/or matrix develop. In some instances the Type II lesion becomes hypermature and due to starvation dies to become a mummified, inert calcified Type III lesion. Type I and II lesions may undergo three types of rupture: contained, communicating and direct. Contained rupture is clinically silent, but communicating rupture may cause biliary obstruction and evacuation or infection of the cyst. Direct rupture has the greatest clinical consequences which include anaphylaxis, dissemination of hydatid disease (secondary hydatosis) within the host, and bacterial infection of the pericyst cavity. The clinical implications of the hydatid disease at different stages are discussed. A plea is made for the development of an international medical hydatid registry employing uniform nomenclature and consistent reporting in order to allow more rational comparisons of different types of management. Lewall, D. B. (1998). Clinical Radiology 53, 863-874. Hydatid Disease: Biology, Pathology, Imaging and Classification

Hydatid disease is a major medical problem in many parts of the developing world (Fig. 1), but less so in the developed world. The prevalence is unknown because many - possibly most - cases are undiagnosed and because of under-reporting. The disease is often managed more effectively in the developing world where it is known than in the developed world where it tends to be an exotic intruder [1]. In this review only cystic hydatid disease caused by Echinococcus granulosus will be considered; the geographical distribution, biological behaviour and treatment of E. multilocularis are different. Although the term 'hydatid cyst' is not, strictly speaking, correct, it has been sanctioned by ahnost universal usage and will be used here. Hydatid disease is unusual in that rupture and its sequellae (biliary obstruction, infection, dissemination and anaphylaxis) are more important than the mass effect of the cyst, despite the enormous size sometimes attained by the lesion. The natural progression from simple to complex cyst, and then to senescence and death, as well as rupture and its sequellae can be imaged noninvasively by ultrasound (US), computed tomography (CT) and magnetic resonance (MR), and in some instances by plain radiographs. Hydatids in the liver have a structure similar to lesions in other sites, but the host reaction (pericyst), which plays a rote in the development of the cyst is particularly intense in the liver. The gross appearance of hydatid cysts, even after rupture, is often appreciated better by the radiologist than by the pathologist who usually receives only fragments of tissue. This review will consider mainly disease in the liver and lungs as these are the most frequently involved organs. Of at least 20 classifications that have been proposed a few stand out [2-13]. However, as most are based on imaging rather than on the actual Correspondence to: Dr D. B. Lewall, Comes de Rull, Casa C, Sispony, Andorra, Spain. 9 1998 Tile Royal College of Radiologists.

pathology of the lesion, they are often not helpful in making outcome comparisons, nor are they ideal for planning surgical, interventional or medical treatment. A problem that has vexed attempts at classification for over three decades is that as imaging has improved classifications have changed. A pathology-based system should get around this difficulty. The use of percutaneous drainage in addition to established surgical and medical treatment increases the need for a consistent system of classification. In this paper the pathophysiology of hydatid disease is reviewed and a pathology-based classification with imaging correlation is presented.

L I F E CYCLE The principal host is a carnivore such as the dog or wolf, and the intermediate host is a herbivore such as the sheep or camel. Humans are accidental intermediate hosts. A high degree of host specificity has been noted in the primary, but not in the intermediate host. The domestic cat, for example, does not play a role as a primary host. The reasons for this poorly understood specificity may include the microtopography of the intestine, biochemical and immunological factors or the composition of the host's bile [14]. The primary host carries a large number of the adult flatworms (averaging 4 mm in length) in the proximal small bowel. The intermediate host ingests eggs of E. granulosus which are excreted in the faeces of the primary host. Proteolytic enzymes digest the protective covering of the ingested egg, releasing the oncosphere which attaches to the jejeunal mucosa by hooklets and suckers. Oncospheres burrow into the submucosa by means of rhythmic muscular movements involving the body and hooklets, aided by secretions of the so-called penetration gland [15]. Oncospheres then enter

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Fig. 1 - Distribution of cystic echinococcus. Note that this is not principally a tropical disease. The highest frequency is in South America, North Africa, the Mediterranean littoral, Eastern Europe, and the Middle and Far East. The disease has been partially controlled in some areas which previously had a high incidence, such as Australasia, Greenland and Cyprus.

veins or lymphatics and those that travel in the portal system arrest in the capillary bed of the liver, while those that travel in lymphatics are thought to bypass the liver to end up in the lungs, brain, bone and other sites. Inhaled eggs can also cause pulmonary hydatid disease as it has been shown that eggs administered to sheep via a tracheostomy develop into lung cysts [16]. The encysted

oncosphere grows 1-5 cm in diameter per year, depending on the density of the host tissue. The cyst produces protoscolices which are released when a carnivore ingests the viscera of the intermediate host. The swallowed protoscolices evaginate to become scolices which attach to the proximal small bowel, completing the life cycle (Fig. 2).

Adult worms in small bowel

Protoscolices ~ evaginate and attach to small bowel

f

Q

Cyst eaten by carnivore, releasing protoscolices

9

Eggs passed in faeces are ingested by herbivore

i Hatch into oncospheres which enter veins and lymphatics

Encyst in liver, lung, etc. and produce Fig. 2 - The life cycle of Echinococcus granulosus. 9 1998 The Royal College of Radiologists, ClinicalRadiology, 53, 863-874

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(a) Fig. 4 - Transverse CT scan through liver showing Type I hydatid cysts. Hydatid sand, composed of brood capsules and scolices, settles to the dependent portion of the cyst but it cannot be resolved on CT images. However, sand can be shown by US if the patient is rotated immediately before scanning so that the settling particles resemble a snow storm. Uncalcified pericyst and intact endocyst in intimate contact with the pericyst are not visible, but after rupture, detached endocyst becomes visible by CT and US (see Fig. 18). Note dilated pericystic ducts (arrows).

(b) Fig. 3 - (a) Removal of endocyst from the opened pericyst of a lung hydatid. The white endocyst is fragile and easily torn. When the surgeon opens the endocyst and hydatid fluid escapes the endocyst falls away from the pericyst (arrow), as it does when a cyst ruptures. The surgeon must search for and oversew perforating bile ducts during endocystectomy of liver lesions to prevent the development of cysto-biliary fistulae. Perforating bronchi are usually not ligated. (b) Microscopic section of endocyst showing laminated membrane (right) lined on its inner surface by the nucleated germinal layer (arrows) which produces brood capsules and scolices. One scolex is intact but the others have been sectioned. Linear fragments of a disintegrated brood capsule from which scolices were released are seen inferiorly (haematoxylin & eosin stain; original magnification x 250).

PATHOPHYSIOLOGY The encysted oncosphere develops a delicate monocellular inner germinal layer which secretes a PAS-positive polysaccharide protein complex, the acellular laminated layer. This, the endocyst, grows up to 2 mm in thickness (Fig. 3a,b). Even though the laminated layer is quite delicate, it serves to protect the even more fragile germinal layer which lies on its inner surface. The endocyst is the true wall of the cyst. The germinal layer produces clear fluid which attains a pressure of up to 80 cm of water, keeping the endocyst in intimate contact with the pericyst [17,18] (Fig. 4). Hydatid fluid has similar Hounsfield values to water and because the cyst is avascular these values do not change after intravenous contrast enhancement. The endocyst receives its sustenance from the pericyst. Although hydatid fluid has been studied extensively [19-22], the mechanisms by which fluid and other substances are transferred into the avascular cyst are not 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

well understood. However, it is certain that transfer does take place as host proteins and some lipids that are not synthesized by the Echinococcus organism are found in the cyst fluid [22]. Diffusion, endocytosis, specific filter or transport mechanisms, and fissures in cyst membranes have been suggested to explain transport. The evidence for fissures is not convincing. The germinal layer produces brood capsules which release protoscolices. After ingestion by the primary host the head of the protoscolex evaginates and the larva is then referred to as a scolex. This semantic distinction is not usually made in medical writing and both forms are referred to as scolices. Brood capsules and scolices together form hydatid sand, which is just visible to the naked eye. Scolices, which are infectious miniature adult tapeworms, possess a dual potential. If they are ingested by a primary host the apical region of the scolex (suckers, rostellum and hooklets) evaginates and the organism attaches within a crypt of Lieberktihn in the proximal small bowel where it develops into the adult worm. However, if the scolex is deposited in a favourable millieu such as the peritoneal cavity or tracheobronchial tree after cyst rupture it may form a new hydatid cyst [23]. The laminated membrane, which has the texture and fragility of cooked egg white, is not elastic and yet its surface area increases and it becomes thicker as the hydatid sphere enlarges. It is not clear how such an acellular structure accomplishes this but presumably laminations are laid down to accommodate growth and repair. The liver adjacent to the cyst mounts a chronic inflammatory reaction. As this subsides hepatic histiocytes lay down collagen, forming the tough host-derived pericyst (ectocyst) which protects the fragile hydatid cyst much as a tyre protects an inner tube (Fig. 5a,b). The pericyst, which is not demonstrable by US or CT unless it is calcified, becomes thicker as the cyst enlarges. The pericyst around lung lesions is always quite thin, probably because the lung is less dense than liver. The thin pericyst accounts for the typical umbilication or notching of enlarging lung hydatids where they contact bronchi and blood vessels (Fig. 6). Blood vessels are always obliterated within the

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(a)

(a)

(b) (b) Fig. 5 - (a) Transverse scan through liver showing Type II hydatid with matrix (curved arrows) and daughter cysts. The pericyst is seen only where it is calcified (broad arrow). Pericyst calcification is usually neither as dense nor as asymmetrical as in this instance. On T2 weighted MR images the pericyst, whether calcified or not, appears as a zone of decreased signal intensity. (b) Photomicrograph of pericyst. Note hepatocytes in upper left comer. The highly cellular lymphoplasmacytic infiltrate contains bile ducts (large arrows) but not blood vessels. Collagen (bottom right), which is the toughest part of the pericyst, lies nearest to the parasite. The pericyst in the sampled region is not calcified (H & E; original magnification x 250).

Fig. 6 - Umbilication of lung lesions is the result of unyielding vessels and bronchi which indent the expanding but compliant cyst. Detail from lateral view o f chest. The anterior cyst is umbilicated (arrow).

Fig. 7 - (a) Type II hydatid cyst in a sectioned spleen. Daughter cysts which are imbedded in matrix originally completely filled the impressions in the matrix; the gaps between the two are artefactual due to dehydration of the daughters during formalin fixation. This is a hypermature lesion which probably would not have ruptured (see text). (b) Photomicrograph of matrix (same patient). Note the folds of laminated membrane (long arrows), vestiges of scolices (short arrows) and hooklets (arrow head), all in advanced stages of degeneration (H & E; original magnification x 250).

Fig. 8 - Transverse US scan of a liver hydatid showing pseudo-tumoral appearance due to the abundance of echogenic matrix. The margins of the hydatid were defined by the sonographer with crosses. The fluid-conlalning daughter cysts (arrows) indicate the true nature of this hypermature Type II cyst. 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

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developing pericyst, but bile ducts and bronchi are not [24,25]. Eventually the increasingly substantial pericyst becomes a hindrance to further enlargement of the endoc y s t , f o r c i n g it to b e c o m e r e d u n d a n t w i t h i n t h e c o n f i n e s o f the pericyst. Those parts of the endocyst that become

Fig. 9 - CT scan through true pelvis showing Type III hydatid. This was judged to be dead as the endocyst of both the daughter and mother are calcified and the lesion has an irregular, nonspherical outline. Intraperitoneal hydatids evoke very little pericystic reaction because they do not compress host tissue as they do in the liver (Fig. 12). Thus, the peripheral calcification in this lesion is mainly endocystic, not pericystic. The indirect haemagglutination test for hydatid was negative and the lesion was not removed. In time it will probably become smaller and more densely calcified, to resemble the lesion in Fig. 10.

Fig. 12 - CT scan through kidneys showing exophytic Type I cyst of the right kidney.

Fig. 10 - Type III lesions are not normally resected, but as this one protruded beyond the liver edge it abraded the peritoneum as the patient breathed, causing pain. Left: external surface. Right: cut surface showing calcified matrix. Note the calcified laminated membranes (arrows). The remaining matrix which is composed of older, more degenerated and heavily calcified membranes no longer has any discernible structure. The lesion was stony hard and had to be sectioned with a saw.

Fig. 1 3 - Opened Type I intraperitoneal hydatid. Note the thin pericyst (arrows) formed mainly of fibrous tissue. The pericyst of intraperitoneal hydatids is so insubstantial that it is unwise to treat such lesions by percutaneous puncture for fear of provoking direct rupture. Purely medical treatment may be safer (see text).

Fig. 11 - Transverse CT scan through liver and spleen showing hypermature Type II hydatids in both organs. Note dilated ducts anterior to the liver cyst.

Fig. 14 - CT scan of head showing a Type I orbital hydatid cyst. The orbit is expanded but bone is not destroyed. The child arrived at the hospital with her eyelids sutured together (arrows).

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Fig. 15 - Hydatid of the pelvic bone. Although the bone is expanded and destroyed there is no evidence of attempted repair. The lesion crossed the hip joint and involved the femoral head (proven by CT and surgery).

isolated from the nourishing hydatid fluid degenerate, forming a gelatinous amber-coloured structure called matrix (Fig. 7a,b) which may have a pseudo-tumoral appearance on CT or US (Fig. 8) [26,27]. Because matrix has an amorphous yellow appearance, it can be confused with pus by the surgeon [18]. Matrix has been neglected in the veterinary literature, presumably because domestic animals are slaughtered while young, before matrix has a chance to develop. On the other hand, hydatids often coexist with their human hosts for many years. Matrix is most common in older patients who on average have harboured the parasite longer than the young [6]. Lung lesions usually do not develop matrix, probably because enlargement of the cysts is relatively unrestricted until they become big enough that further growth is inhibited by the chest wall, mediastinum or diaphragm. Cysts and pericysts in the lung never calcify, but it is not known why. Cysts in other sites, including the mediastinum and pericardium, may calcify. Calcification of the pericyst, which can occur at all stages of the life cycle of hydatids, is found in nearly one-third of liver cysts. Pericyst calcification does not indicate that the cyst is dead, but calcification of the cyst itself does (Figs 9 and 10). Lesions in the spleen (Fig. 11) and kidney (Fig. 12) usually have a structure similar to those in the liver. Cysts in the peritoneal cavity elicit little pericyst reaction because they grow without compressing

surrounding host parenchyma which is the main source of pericyst tissue (Fig. 13). Brain cysts tend to be discovered before they develop daughters and matrix. Because they evoke little host reaction, brain lesions have an insubstantial pericyst [28,29]. Orbital hydatids cause unilateral exophthalmos and, if untreated, slowly compress the globe and enlarge the bony orbit, causing unilateral blindness [30] (Fig. 14). Bone cysts occur most often in the pelvis, vertebral column, long bones and skull and cause destruction without evoking bone reaction. A true pericyst develops only if cortical erosion allows soft tissue involvement to occur [31]. This accounts for the often bizarre appearance of bony hydatids and possibly for their unusual propensity to cross joints and involve adjacent bones (Fig. 15). Daughter cysts, which are thought to develop from scolices, are produced either synchronously with matrix or they may appear first. It has been suggested that they form in response to a threat to the continued existence of the mother [24]. Daughters replicate the structure of the mother cyst, but they do not stimulate production of their own pericyst as they are not in contact with host tissue. Cysts with a predominance of daughters are often mistakenly described as being septated (Fig. 10) but what appear to be septa in fact are the opposing walls of daughters which are flattened by contact with each other. When the daughters are removed the 'septa' disappear. Daughters occasionally contain granddaughters. All hydatid lesions start as purely cystic Type I structures (Figs 4, 12 and 14), and if they develop daughter cysts or matrix (or both) they are termed Type II cysts (Figs 7a, 8, 9, 10 and 11). When formed elements completely replace the nourishing hydatid fluid, the Type II lesion is starved, dies and eventually becomes a calcified and biologically inert Type III lesion [6] (Figs 9 and 16). When the only remaining hydatid fluid is in daughter cysts, the lesion can be considered hypermature as it is probably nearing death by starvation (Figs 5, 7a, 8 and 11). The foregoing, which can be regarded as the natural history of hydatid cysts in the intermediate host, is often modified by rupture which may cause biliary obstruction, infection, dissemination and anaphylaxis, all of which are more important than the mass effect of the lesion. Most hydatids develop in the liver (60-70%) and lung (15-20%). However, they are encountered in virtually every organ and tissue. Type I lesions are more frequent than Type II lesions. The incidence of Type III lesions is unknown as these are usually without clinical importance and are not recorded, but personal experience suggests that they are the most common type. Lesions are twice as likely to be solitary as multiple and multiorgan involvement occurs in 10-15% of cases. The progression of hydatids from simple to complex is shown schematically in the column on the left side of Fig. 17. COMPLICATIONS

Rupture The causes of rupture include trauma, medical treatment and endocyst degeneration. Three types of rupture are possible: contained, communicating and direct [7].

Contained Rupture Fig. 16 - CT scan of the liver showing Type II lesion with predominance of daughter cysts. The 'septa' are the walls of daughter cysts flattened by contact with other daughters.

This occurs when the endocyst ruptures in a lesion in which patent biliary radicals (or bronchi in the case of 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

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Maturation and senescence

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Rupture I

I

\

Communicating

/

Direct

Prematu re death and/or infection

III

Fig. 17 - Schematic representation of the natural history and complications of hydatid cysts. Cysts which have undergone contained rupture may die, but they do not become infected. The pericyst may calcify at any stage of maturation of the lesion and does not imply that the lesion is dead. However, calcification of the endocyst and its contents is proof that the parasite has died.

pulmonary lesions) do not penetrate the pericyst (Fig. 18). The actual incidence of contained rupture is unknown as it is asymptomatic and is diagnosed fortuitously when sectional imaging shows floating membranes within the hydatid lesion. Lung hydatids are often not imaged by CT or MR and virtually never by US so contained rupture of lung lesions is probably under-diagnosed. Contained rupture does not invariably cause premature death of the cyst and does not predispose to secondary bacterial infection (see below).

pericyst and allow herniation of a small knuckle of delicate e n d o c y s t m a y p r e d i s p o s e to r u p t u r e [33]. B e c a u s e o f t h e p r o p e n s i t y o f l u n g c y s t s to r u p t u r e , s u r g e o n s u s u a l l y o p e r a t e o n l u n g l e s i o n s b e f o r e t h e y a t t e n d to t h o s e i n t h e liver if the patient has both. Sectional imaging of liver cysts which have undergone communicating rupture demonstrates detached endocyst floating in the remaining

Communicating Rupture Communicating rupture is possible when biliary radicals or bronchi perforate the pericyst in the liver or lung [7,24] allowing fluid and formed elements to escape into the biliary or bronchial tree. Communicating rupture in the lung leads to expectoration of salty fluid and sometimes of fragments of endocyst which the patient describes as 'grape skins'. If air enters the partially evacuated pericyst cavity, the water lily sign will be seen on upright chest radiographs. Communicating rupture seems to be proportionately more common in the lung than in the liver, presumably because of a higher incidence of bronchial than biliary patency through the pericyst. This is probably because bronchi are more robust than bile ducts and are less likely to be obliterated by the developing pericyst. Communicating rupture of lung cysts does not always kill the parasite [32]. Dilated bile ducts which perforate the 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

Fig. 18-Transverse CT scan through liver showing ruptured Type I hydatid cysts. The child was treated medically with an oral antihelminthic which killed the cysts and caused spontaneous rupture. Because the cysts did not become smaller and there was no evidence of biliary obstruction, the rupture was assumed to be contained. Purely medical treatment is generally avoided because of the danger of provoking communicating or direct rupture (Fig. 19a,b). This patient was lost to follow-up.

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(a)

(b) Fig. 19 - (a) Longitudinal US scan of liver showing Type I cyst prior to treatment. (b) Transverse scan after treatment with an oral antihelminthic which caused the cyst to rupture. The fact that the cyst became smaller and less spherical proves that this is a communicating rupture even though dilated bile ducts are not demonstrable. Note the detached endocyst on this transverse scan. A few days after this examination the patient developed biliary obstruction and required surgery.

cyst fluid - the sectional imaging counterpart of the water lily sign. The cyst may become appreciably smaller and less spherical (Fig. 19a,b), and there may be evidence of downstream biliary obstruction. Communicating rupture may be diagnosed directly, by the demonstration of hydatid debris in the biliary tree [34] or air in a lung cyst, or when contrast enters the cyst cavity during endoscopic retrograde cholangiopancreatography (ERCP) (Fig. 20). Communicating rupture occasionally presents with a f a t fluid level in the cyst cavity [35]. Dilated pericystic ducts, which are apparent in 25% of liver hydatids, are usually much more tortuous than blood vessels. A clear distinction between the two is possible only if CT scans are performed with intravenous contrast enhancement (Fig. 4) - a distinction that is not as easy on US examinations. Dilated bile ducts in the unruptured hydatid are always upstream (in terms of bile flow) of the cyst. The reasons for biliary dilatation and biliary perforation of the pericyst are probably related. Dilated ducts have been shown to be either tangential or radial to the cyst and it has been postulated that the latter develop from the former. Tangential ducts do not communicate with the potential space between endocyst and pericyst, whereas radial ducts do. Tangential ducts which are incorporated into the pericyst are

Fig. 20 - ERCP showing connection between the biliary tree and a Type II cyst. During prolonged medical treatment before intended elective surgery the cyst ruptured and the patient developed biliary obstruction, Urgent surgery was performed to avoid the development of cholangitis. C: collapsed pericyst. Arrow: communicating bile duct.

presumed to become sufficiently stretched and attenuated by the expanding cyst that the upstream moiety obstructs and dilates. With further growth of the cyst the tangential duct severs, becoming two radial ducts [33]. Unless this hypothesis is shown to be false, dilated ducts should be considered an indication that unseen communicating ducts exist downstream, threatening biliary obstruction after rupture. At the time of rupture small daughter cysts and fragments of endocyst may be forced into the upstream ducts, but they do not cause obstruction as the pressure within the cyst cavity soon drops as hydatid fluid leaves via the downstream ducts. Bile flow then returns the debris to the pericyst cavity. The bile that floods the pericyst cavity probably always kills the parasite. Biliary obstruction, which occurs if formed elements enter downstream ducts, characteristically produces fluctuating jaundice which may even disappear for short periods, presumably because of the compliance of the obstructing fragments [36]. Scolices probably do not survive in the hostile environment of the biliary tree, but scolices that were accidentally spilled into the tracheobronchial tree during resection of pulmonary hydatids were estimated to be the cause of secondary lung lesions in 0.61% of 650 cases [23]. Thus, it is likely that spontaneous communicating rupture of lung cysts can lead to trans-bronchial spread of hydatid disease. The distinction between contained and communicating rupture is not always possible [7]. 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

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Fig. 21 - Transverse CT scan through false pelvis showing late sequel of spontaneous direct rupture into the peritoneal cavity. Secondary Type I and II cysts developed from scolices that spilled into the peritoneal cavity.

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Fig. 2 2 - Transverse US scan of liver showing prematurely dead Type I hydatid cyst. The appearance is identical to that of an infected hydatid cyst.

Infection Direct Rupture Direct rupture, which can have disastrous consequences, occurs when both endocyst and pericyst are torn. This usually happens to lesions near the edge of the liver where the protective pericyst may be deficient and where there is little host tissue to offer support [33]. The thin pericyst and compliant lung parenchyma around lung cysts offer relatively poor protection to the endocyst. Fluid and infectious scolices spill into the peritoneal or pleural cavity causing seeding (Fig. 21) and, often, anaphylaxis. Direct rupture has been reported into many sites including the liver [37] pleura [38], lung [7], gastrointestinal tract [39] and great vessels [40]. Direct rupture into soft tissues almost certainly explains the development of small satellite lesions around a cyst [37,41,42]. This type of rupture probably accounts for most reports of recurrence after surgery. Other causes of 'recurrence' are small lesions that were not detected pre-operafively, and growth of new lesions resulting from spillage of scolices during surgery [41]. More complex explanations of recurrence such as exophytic growth do not seem tenable on biological grounds because there is no germinal layer on the outside of the endocyst [24,42,43]. Bulging of part of the wall of the mother cyst which is sometimes seen when cysts are near the edge of the liver or when they abut a fissure must not be confused with exophytic budding [33]. Biliary obstruction is usually not a feature of direct rupture because the cyst is quickly decompressed and solid elements are not forced into downstream ducts [33]. Anaphylaxis is much more frequent after direct rupture than after communicating rupture, apparently as a result of the interaction of antigenic hydatid fluid and a serosal surface [44]. Direct rupture usually leads to premature death of the cyst (see below) and theoretically can result in bacterial infection of the pericyst cavity. Hydatid cysts in any site which result from rupture are termed secondary cysts (Fig. 21). Most pleural cysts result from direct rupture of lung hydatids into the pleural space or from rupture of liver cysts through the diaphragm. Biliary-bronchial fistulae are a consequence of direct rupture of a liver cyst through the diaphragm and pleural membranes into the lung. The inflammatory reaction elicited by bile in the lung enables the biliary-bronchial connection to be made. Rupture is shown diagramatically in Fig. 17. 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

Infection occurs only after communicating or direct rupture (usually the former) because bacteria-transporting blood vessels do not penetrate the pericyst. Infection associated with communicating rupture and biliary obstruction can result in an abscess within the pericyst cavity [45] or in cholangitis, and probably always kills the parasite. Because of the danger of infection, biliary obstruction must be relieved promptly. Infection leads to a loss of clarity of interior detail of the cyst, and fluid elements become echogenic by ultrasound [46,47], and denser by CT [47,48]. The endocyst is usually seen to have detached from the pericyst, and occasionally gas is produced in the cyst.

Premature Death This is defined as death that is not the result of starvation of a hypermature Type 11 lesion and it may occur after rupture, infection or medical treatment. When a Type I lesion dies prematurely after rupture it may develop directly into a Type 1II lesion. However, a prematurely dead Type I lesion followed for 30months did not calcify (personal experience), so it is possible that such lesions are sometimes eventually resorbed. Unless infection produces gas, premature death and infection have identical appearances on CT and US [10] although they have very different clinical presentations. In both instances the fluid component becomes echogenic by US (Fig. 22) and denser by CT, and there is a loss of clarity of the internal detail of the lesion. With both methods of imaging the endocyst is usually seen to be detached from the pericyst. Premature death apparently does not produce a diagnostic change in the MR signal [49]. Infection and premature death are indistinguishable with current imaging methods. The proposed classification of the natural history and complications of hydatids (Fig. 17) is modified from two earlier classifications [6,7].

S U M M A R Y OF IMAGING

The approach to imaging hydatids depends on the availability of equipment and the site of the lesion. Except for lesions in the lung or brain, conventional radiography and US are often sufficient for diagnosis and management.

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Pulmonary lesions are usually detected on the chest X-ray but when it is available CT is helpful for complete topographic evaluation. Evaluation of Type I and Type II lesions in solid organs requires US and/or CT. If there are many cysts CT is usually preferred by the surgeon. Brain hydatids can be imaged by either CT or MR, but ease of imaging in all planes and detailed depiction of cerebral anatomy with MR make this method particularly useful. Plain films are often adequate for imaging bone hydatids (Fig. 15). Angiography, Doppler sonography and nuclear medicine are rarely useful.

Unruptured Cysts Type I lesions have a non-specific cystic appearance but if the patient is rotated immediately before US scanning the settling hydatid sand produces signals which have been likened to falling snow. Pericyst is not identified by US, and is seen by CT only if it is calcified (Fig. 5a). However, it is demonstrable by MR, particularly on T2-weighted images which produce a low intensity rim. Neither the cyst nor the pericyst enhance by CT or MR as they are avascular [24,50]. Lung lesions are often umbilicated on plain radiographs (Fig. 6). Type H lesions usually have a characteristic appearance due to daughter cysts whether or not fluid or matrix are present (Figs 5a, 8, 11 and 16). Hypermature Type II lesions which lack daughters have a non-specific appearance by US and CT but MR is helpful as it shows the hypointense pericyst. Fluid in mother cysts has the same appearance as it does in daughters by all methods of cross sectional imaging. Type III lesions are often discovered on plain films. They are densely and irregularly calcified and may reveal vestigial evidence of the antecedent Type II lesion (Fig. 10). Discovery of a Type III lesion should provoke a search for uncalcified Type I and II liver cysts.

Ruptured Hydatids Contained rupture makes the detached endocyst visible by all cross sectional imaging methods. The lesion does not become smaller (Fig. 18). Communicating rupture also produces a characteristic separation of endocyst from pericyst, and the cyst becomes smaller (Fig. 19a,b). Biliary obstruction, if it occurs, may result in dilatation of downstream ducts. Occasionally daughter cysts or fragments of endocyst may be seen in the biliary tree by US, CT or MR. ERCP shows filling defects within the biliary tree and may also reveal retrograde communication with the cyst cavity (Fig. 20). If air replaces some of the fluid in the pericyst cavity of lung lesions the water lily sign is produced on upright chest radiographs. Direct rupture of a liver lesion into the chest causes a pleural collection and if a broncho-biliary communication develops it is demonstrable by bronchography or ERCP. Cyst rupture into the abdomen may produce a small amount of ascites and secondary cysts eventually develop in the peritoneal cavity (Fig. 21). Direct rupture of a lung cyst into the lung parenchyma causes a local reaction which has been referred to as pericystic pneumonitis. Rupture into the pleural space induces a pleural collection with or without pneumothorax. After direct rupture cysts in all locations become smaller. Premature death and infection are indistinguishable by US and CT. Hydatid fluid becomes echogenic and daughter cysts become indistinct by US (Fig. 22). Hounsfield values

of fluid increases and detail is lost on CT images. Because it is difficult to distinguish between matrix and pus at surgery [ 18] some lesions that have been reported to be infected may actually have been sterile cysts which contained matrix [2,3,5]. The exact role of MR in assessing infection and premature death is not yet clear. Some have concluded that distinction between cyst death and infection is not possible [10], others contend that it is not possible to distinguish between living and dead cysts [49], and yet others have stated that cysts that are infected or communicate with the biliary tree produce a high intensity proton density signal [50]. The diversity of opinion probably reflects the fact that matrix (which is hyperintense on T2-weighted images) has sometimes been mistaken for hydatid fluid [43,49,50,51 ], or for hydatid sand [51].

CLINICAL IMPLICATIONS Drainage of Type I cysts is gaining acceptance [47,48,52-59] but it should be avoided if pericystic ducts are dilated (Fig. 4) because the inevitable communicating rupture may precipitate biliary obstruction [33]. Even in the absence of visibly dilated ducts, aspirated fluid should be checked for bile and, as an additional precaution, a cystogram may be performed to ensure that the cyst does not communicate with the biliary tree [56]. Communication is demonstrated more often at surgery than by non-invasive imaging, indicating that it is under-diagnosed preoperatively [50,57]. Sclerosing solutions such as formalin or silver nitrate should never be injected into a cyst for fear of causing sclerosing cholangitis [1,60-63]. Moreover, perforating bile ducts carry hypertonic saline to the gut from where it is absorbed, causing hypernatraemia and sometimes congestive heart failure [1,63]. For this reason Cetrimide has become the favoured antiscolicidal agent in most [63], but not all, centres [59]. Percutaneous drainage is not advisable if the cyst cannot be approached through normal parenchyma of the host organ or when the pericyst is insubstantial (Figs 3a, 6, 12, 13 and 21) because of the danger of direct rupture, dissemination and anaphylaxis. Purely medical treatment has been used occasionally when surgery is contraindicated or in widely disseminated disease [64,65], but the patient must be monitored closely because of the danger of communicating or direct rupture. It is possible that direct rupture as a result of treatment of intraperitoneal and similar cysts is a benign process as the ruptured cyst is probably sterile and the fluid probably has lost its antigenicity by the time of rupture. Furthermore, there is no danger of a biliary leak or bleeding after rupture of such lesions. This suggestion must be put to the test in a controlled study before it is accepted. Patients are usually pre-treated for a short time (10-14 days) with an antiscolicidal agent such as Albendazole prior to definitive surgery or percutaneous drainage, and for several weeks after the procedure [59]. An excessive period of pre-treatment is dangerous as it may precipitate communicating or direct rupture (Fig. 20) [33]. Although various surgical methods have their advocates, centres with wide experience tend to favour the most conservative approach - endocystectomy [25,59,63,66-68]. Many authors recommend that Type II cysts should not be drained percutaneously because of the difficulty removing daughter cysts and matrix, although there are dissenting opinions, especially if only daughters are present as they can be punctured individually [47,48,53,56]. Time and experience will tell whether 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 863-874

HYDATID DISEASE

uncomplicated hypermature Type II cysts actually require resection. Hypermaturity is probably a terminal stage prior to death and conversion to a clinically insignificant Type III lesion. Moreover, intuition suggests that hypermature lesions must be physically stable and resistant to rupture, especially if they are surrounded by substantial pericyst and organ parenchyma. The thickness of pericyst is difficult to estimate by CT or US but MR may be useful in this regard. Although hydatid disease is common, individual series are usually not large. For this reason an international medical hydatid registry employing uniform nomenclature and consistent reporting would be valuable for assessing the outcome of various forms of medical, surgical and interventional management. Acknowledgements. I wish to thank Dr Persha Nyak, Consultant Surgeon, and Dr Norman Chan, Consultant Pathologist, King Fahad National Guard Hospital, Riyadh, and Dr Ashraf All, Chairman, Department of Pathology, King Faisal Specialist Hospital, Riyadh, for their advice. My thanks also to my colleagues in the Department of Medical Imaging for their helpful suggestions and to Miss Shirley Bishop for her patience in typing the manuscript.

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