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Liver alveolar echinococcosis in China: Clinical aspect with relative basic research
 
Ci-Peng Jiang, McManus Don, Malcolm Jones
ELSEVIER
PO Box 2345, Beijing 100023, China World J Gastroenterol 2005;11(30):4611-4617
www.wjgnet.com World Journal of Gastroenterology ISSN 1007-9327
wjg@wjgnet.com © 2005 The WJG Press and Elsevier Inc. All rights reserved.
Ci-Peng Jiang, Hydatidosis Research Laboratory of Basic Medical
School, Lanzhou University, Lanzhou 730000, Gansu Province, China
McManus Don, Malcolm Jones, Post Office Royal Brisbane Hospital,
Q 4029 Australia
Supported by England Wellcome Trust, 2002
Correspondence to: Ci-Peng Jiang, MD, Professor of Parasitology,
Hydatidosis Research Laboratory of Basic Medical School, Lanzhou
University, Western Dong Gang Road, Lanzhou 730000, Gansu
Province, China
Telephone: +86-931-8616759 Fax: +86-931-8611355
Received: 2004-09-23 Accepted: 2004-11-12
Abstract
 his paper deals with all aspects of liver alveolar echinococcosis (AE) including epidemiology, pathology, clinical manifestations, imaging examinations, diagnosis and differential diagnosis, surgical treatment and chemotherapy.
The review is not only based on personal clinical experiences but also in combination with relative basic research such as   oliferation and growth of alveococcus, preclinical studies of a novel compound extracted from TCM for treatment of liver AE, and molecular immunology used for specific AE diagnosis, etc.
 
INTRODUCTION
Echinococcosis is a parasitic zoonosis, consisting of cystic echinococcosis (CE) and alveolar echinococcosis (AE). These two types differ in parasitology, epidemiology, pathology, clinical aspects, treatment and prognosis. They are respectively caused by the larval stage of Echinococcus granulosus (Eg) and E. multilocularis (Em) (Figure 1). Over one hundred years,
the disease had been misdiagnosed as liver colloid cancer.The cause of AE was not confirmed until 1856. In China,liver AE was reported respectively in Ningxia, Xinjiang autonomous regions and Gansu Province during 1950s to 1970s[1-3]. Up to now, at least one thousand cases of AE have been reported throughout China, but most of them were mistaken as liver cancer. In order to improve the diagnostic level of AE, a review is comprehensively introduced as follows. 
 
 
 
EPIDEMIOLOGY
Em needs two mammalian hosts for completion of its life  cycle. They are respectively called the definite host, arnivore and the intermediate host, mainly rodents. Proglottid containing eggs or free eggs are excreted in the feces of the
definite hosts, e.g. dog or fox. Once eggs are ingested by the intermediate hosts including rodents and human beings, AE may occur in liver or other organs. In China, fox, dog and wolf have been found to be as definite hosts and a few species of the rodent such as Citellus dauricus, Myospalax fontanieri, Microtus brandti, were confirmed to be as intermediate hosts. Human body affected by AE is chiefly due to contacting the animals: fox, dog, or occasionally cat. Especially, ladies, herdsmen and hunters are higher risk populations. AE has been found mainly in the west of China including eight provinces or autonomous regions Human AE epidemiological survey in three counties of central eastern Gansu  
Positive rate of immuno-test(%)
Yr          County         Persons investigated    Ultrasonic Intradermal  test   ELISA morbidity(%)
1986[6] Zhang County           380                           19.2                                                   2.4
1992[7] Zhang County                             1 312                          2.8                                 5.0
1998[8] Ming County             1 200                                                                2.2            5.6
2003[9] Lintao                        1 071                                  1.8                                               7
 
PROLIFERATION AND GROWTH OF ALVEOCOCCUS AND HISTOGENESIS OF PROTOSCO LEX
  Proliferation and growth of alveococcus is very significant
as it bears practical relation with clinical aspects especially chemotherapy. As early as in 1950s to 1980s, a few Euroamerican
authors[16-21] observed the proliferation and growth phenomenon of experimental alveococcus respectively in white
mice, cotton mice, and jirds (Meriones unguiculatus). Our study was partially carried out microscopically on the pathological
sections of human AE[22]. Two modes of proliferation were found, i.e. endogenous budding and exogenous budding
The former was characterized by internally protrusive hyperplasia from the mother alveolar
wall into the alveolar cavity and then proliferation extending continuously to reach the opposite wall of the cavity. So,
septum-like budding was named. Sometimes two or more proliferative sites on the alveolar wall propagated simultaneously
into the cavity in opposite directions, and mingled with each other to form a septum dividing the mother to form two or
more small alveoli Externally protrusive proliferation occurred at one or several sites of the mother
alveolar wall, producing single or multiple daughter and granddaughter alveoli under the name of exogenous budding
These two buddings may coexist not only in one Jiang CP et al. LAE in China 4613 section of liver AE but also in that of metastatic lung or          brain AE and metastatic lymph node AE. To date, the mechanism of AE proliferation and growth is not understood completely although it has been studied for decades. In the exogenous proliferative course of liver AE, the daughter alveoli of 1st grade budding and the granddaughter alveoli of 2nd grade budding were respectively named. Proliferating grade by grade, a mother alveolus may propagate into numerousnew alveoli of multi-grades just like infiltrative dissemination of carcinoma, or it further affects neighbouring organs such as porta hepatis, inferior vena cava or pancreas, rendering radical surgical operation impossible. Euzeby[21] explained that exogenous budding was due to discontinuity of the alveolar cuticular layer, allowing the germinal membrane to escape from the mother alveolus .As concerns the entire
process of protoscolex histogenesis, a stage of the formation of brood capsule must be passed through. Local cellular hyperplasia began in the wall of brood capsule, and elliptical, mushroom-shaped or lingual protrusion protruded into the cavity of brood capsule. After that, the protrusion gradually developed into rostellum and suckers, finally changing from
embryonic protoscolex to mature protoscolex of evaginated or invaginated type .The formation of brood capsule expressed two modes. The first was local hyperplasia of germinal membrane of alveococcus wall, forming cellular group.
By means of cellular rearrangement, the cells accumulated towards the periphery and a cell-free space appeared in the center, developing further into brood capsule[23] (Figure 5). This is basically similar to other reports at home and abroad[19,25].
The second mode of brood capsule formation was found by us from liver AE of Mus musculus in Zhang County, Gansu
Province[24] (Figure 6). Similar report has not been seen yet. 
 
PATHOLOGY Macroscopical appearance
The lesion was yellowish or gray and felt as firm as cartilage. Superficially, it showed numerous noduli or minute cysts
without definite encapsu-lation, but with alveolate structure on cross section . It was usually classified into
three types, of which large circumscribed mass type was more common (67.8%) and the other two were nodular
type (16.7%) and mixed type (15.5%) [26]. The central area of alveococcus may be complicated by
coagulated necrosis due to poor blood supply. Microscopic finding The lesion was characterized by many
alveoli with different sizes and shapes. Observation of alveolus wall showed that the thick, acellular, laminated outer layer
looked bank-like, sometimes folding within the alveolar cavity. The thin, germinal inner membrane lined by a singlelayer cell was usually deficient due to detachment. Brood capsule or protoscolices were occasionally seen . The lesion may be complicated by central necrosis, producing a cavity or pseudocyst after liquidization. In the periphery of alveoli group it showed hyperplasia of fibroconnective tissue and cellular infiltration of eosinocytes,lymphocytes, plasma cells and giant cells, forming a typical alveococcus nodule .Metastasis According to a collective analysis of 270 cases with liver AE from five provinces of China[27],
general metastatic rate was 3.7%(10/270). The commonest metastatic organ was lung (4.7%)and the next one was brain (3.3%) .
Three modes of metastasis were found. The first was direct infiltrative dissemination. The alveococcus lesion infiltrated gradually into the liver parenchyma and formed a large mass. The neighbouring organs outside the liver such as the porta hepatis, diaphragm, pancreas or inferior vena cava were further involved. The second was blood metastasis.
A small portion of detached proliferating bud, if involving the branches of portal vein, extensively disseminated within the liver parenchyma resulted in multiple noduli. Involving the branches of hepatic vein, the alveococcus spread along systemic circulation to distal organs such as lung or/and brain. The third was lymphatic metastasis. The liver alveococcus
may spread to lymph nodes of the porta hepatis . peritoneal cavity and colonic mesentery. According to the results of animal experiment in Japan[28], the mechanism of metastasis was due to the detached proliferated bud, even
very small or only a few nuclei entering the blood vessels. Nevertheless, it was incapable of causing metastasis if protoscolices were injected into the vessels. 
 
CLINICAL MANIFESTATIONS
Generally speaking, sex difference is not obvious, sometimes males slightly outnumbered females. Most patients were
young and in robust years of their life. According to clinical features[29], four types, i.e. simple hepatic enlargement,
obstructive jaundice, liver giant node (cancer-like) and remote metastasis were classified. According to clinical
course, we divided AE into the early stage with only mild hepatic enlargement, middle stage with progressive  hepatomegaly
and the advanced stage associated with impaired liver function, portal hypertension, or metastasis[30]. The main
symptom was upper abdominal mass or liver mass with stiff and nodular feeling on palpation. The size of the mass
varied, with the smallest being not felt or only palpated below right sub-costal margin and the largest reaching the 8A
umbilicus level (Figures 8A and B). Another symptom was abdominal pain, but usually not severe. Jaundice was found
in some cases, usually due to the impairment of liver function or the invasion and compression of bile duct by                 
liver mass at the advanced stage. Extensive infiltration of the alveococcus lesion or fibrosis caused liver cirrhosis with
subsequent portal hypertension such as the superficial varicosity of the thoracic or abdominal wall, ascites and
splenomegaly. In case of liver AE associated with lung or brain metastasis, the patient manifested corresponding
respiratory or neuropathic symptoms and signs.I
 
MAGING EXAMINATIONS (Figure 9) X-ray films
Enlargement of liver and elevation of right diaphragm were shown on abdominal plain film. The shadows of spotted or            
clustered calcification were visible in the hepatic region. But they must be carefully observed as their appearances were
usually not distinct. If multiple shadows of bilateral lung showed on chest film, the possibility of liver AE associated   
with lung metastasis ought to be considered.
 Ultrasonic scanning In a series of 141 cases with liver AE[31], the ultrasonic features                9
revealed solid mass in 96 and solid-cystic degeneration in 45. The former comprised 23 cases with local type, 21 with diffuse nodular type and 52 with large circumscribed masstype. If the liver alveococcus was complicated by central necrotic pseudocyst, the ultrasonic scanning showed echofree area with irregular cystic wall .
 
Computerized tomography (CT)
Liver CT showed single or multiple, intrahepatic, hypodense areas with irregular margin, or occasionally partial calcification of alveococcus (Figure 9).
 
IMMUNOLOGICAL EXAMINATIONS
As hydatid intradermal test was simple and cheap, it was commonly used, especially in our country. Although the sensitivity was high, false positive reaction may occur. Therefore indirect hemagglutination test and ELISA were reliable methods for immunological diagnosis due to their higher specificity. Along with current advancement of molecular immunology, purification of a specific antigen from Echinococcus multilocularis (Em) has been successful.  As early as in 1983, Gottstein et al.[32,33], prepared an antigen fraction (Em2) from alveococcus tissue using affinity chromatography. Owing to a high specificity of Em2 for E. multilocularis, a correct serological differential diagnosis was achieved in 95% of 57 confirmed cases of human CE or AE. However, Em2 was isolated from laminated layer of alveococcus, a higher or lower level of antibody titer did not reflect whether the focus was active or not. Em2- ELISA test still showed positive result with a high titer even though the focus became stable or calcified after chemotherapy.As the protoscolex is the most active component of the alveococcus tissues, it was used to isolate protoscolex antigens designated as Em16 and Em18 using Western blotting in a
cooperative study between China and Japan[34]. Em18 and Em16, especially the former showed not only a higher sensitivity but also stronger specificity for immunodiagnosis Jiang CP et al. LAE in China 4615 of human AE. We also used the alveococcus protoscolices for isolating Em16 and Em18 by isoelectric focusing analysis [35]. These protein antigens could not show the best diagnostic value and cross reaction which possibly occurred between AE and CE or between AE and cysticercosis[36]. In short, molecular immunological diagnosis for human AE needs further studies.
 
DIAGNOSIS
Until now, liver AE is always mis-diagnosed. To make a correct diagnosis of liver AE, we should not ignore the past histories of the patients. First, where did the patient come from, AE endemic area? Next, did the patient contact dog, cat, or fox-fur? Thirdly, what is the occupation of the patient, fox-hunter or dog-raiser? These data would be helpful for the diagnosis of liver AE.
 
DIFFERENTIAL DIAGNOSIS
Liver cancer
In our collective review of 274 cases with liver AE, the determination of serum AFP was negative in all the patients[27]. So it is significant for differential diagnosis of AE. As a rule, liver AE pursues a slow, but progressive course.
It obviously differs from liver carcinoma which develops faster or very rapidly, leading to patient death in a short time. AFP test is a reliable differential diagnostic method. Sometimes, gross findings of liver AE may be confused with carcinoma on the operation table and frozen section is necessary. When the diagnosis of liver AE is still difficult before operation, liver needle biopsy may be considered (Figure 10). Occasionally liver AE also needs to be differentiated from cystic echinococcosis (CE) or some nonparasitic diseases such as tuberculosis. If chest X-ray film showed multiple shadows of bilateral lung or brain CT showed cerebral lesion, it might be possible that liver AE was associated with lung or/and brain metastasis[37]. Clinically unknown nature of malignant tumor was always determined.
 
TREATMENT
Surgical operation
The rational treatment for liver AE is radical hepatectomy and the prognosis of the patient may be good. An individual case had been postoperatively followed up for 21 years without recurrence[2].
 However, the rate of hepatectomy is very low due to the difficulty of early diagnosis. According to our collective analysis of 258 cases of liver AE in China[27], only 27(10.5%) and 16 (6.2%) had performed radical liver lobectomy and partial hepatectomy respectively. In order to increase the percentage of hepatectomy, an epidemiological survey in AE endemic area is very significant to screen out early cases. For liver unresectable case, a palliative operation may be indicated such as surgical drainage for a large pseudocyst in order to decompress pericystic liver tissues. As in Figure 8A, the patient was alive for 23 years after external drainage of liver pseudocyst.
Chemotherapy
Albendazole (ABZ) is considered by WHO as the best anti-AE drug. Experimental studies showed that ABZ was able to inhibit alveococcus proliferation and growth. Considering the clinical effects, it was shown to alleviate the symptoms, to prolong the survival, and diminish lung or/and brain metastasis after therapy. In our 23 cases of liver AE treated with ABZ, symptoms were improved, appetite increased, jaundice relieved, and liver enlargement decreased in 15 (65.2%)[38] cases. Liu et al.[39], reported that in 11 cases of liver AE followed-up for 2-7 years after long-term continuous ABZ therapy, 7 showed calcification on liver CT film. Thus ABZ may be lethal to the parasite.
In addition, we found a novel compound extracted from traditional Chinese medicine, Xiao-Bao capsule for treatment of AE. Experimental results showed that the inhibitory rate of mouse AE was 65.7% and 80.6% respectively in two
groups of mice, i.e., 1-week and 10-weeks after innoculative infection[40]. In our 21 cases of liver AE, symptoms improved in 16 (76.1%)[27] cases. Both acute toxicity test in mice and chronic toxicity test in rats showed no toxic reactions[41]. We
postulate that combination of Xiao-Bao capsule and ABZ would be more effective than single medication.

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