• View in gallery
    Figure 1.

    Flow chart of cystic echinococcosis epidemiology systematic review.

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    Figure 2.

    Flow chart of cystic echinococcosis clinical manifestations systematic review.

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    Figure 3.

    (A) Abdominal ultrasound-based frequency of cystic echinococcosis in endemic areas of China (all ages) NHAR = Ningxia Hui Autonomous Region, XUAR = Xinjiang Uygur Autonomous Region. (B) Abdominal ultrasound-based frequency of cystic echinococcosis in endemic areas of Peru (all ages). (C) Abdominal ultrasound-based frequency of cystic echinococcosis in an endemic area of Argentina (school children).

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    Figure 4.

    Portable thoracic radiograph-based frequency of cystic echinococcosis in endemic areas of Peru.

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A Systematic Review of the Literature on Cystic Echinococcosis Frequency Worldwide and Its Associated Clinical Manifestations

Christine M. BudkeDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Hélène CarabinDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Patrick C. NdimubanziDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Hai NguyenDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Elizabeth RainwaterDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Mary DickeyDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Rachana BhattaraiDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Oleksandr ZeziulinDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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Men-Bao QianDepartment of Veterinary Integrative Biosciences, College of Veterinary Medicine, Texas A&M University, College Station, Texas; Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; Department of Health Promotion Sciences, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

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A systematic literature review of cystic echinoccocosis (CE) frequency and symptoms was conducted. Studies without denominators, original data, or using one serological test were excluded. Random-effect log-binomial models were run for CE frequency and proportion of reported symptoms where appropriate. A total of 45 and 25 articles on CE frequency and symptoms met all inclusion criteria. Prevalence of CE ranged from 1% to 7% in community-based studies and incidence rates ranged from 0 to 32 cases per 100,000 in hospital-based studies. The CE prevalence was higher in females (Prevalence Proportion Ratio: 1.35 [95% Bayesian Credible Interval: 1.16–1.53]) and increased with age. The most common manifestations of hepatic and pulmonary CE were abdominal pain (57.3% [95% confidence interval [CI]: 37.3–76.1%]) and cough (51.3% [95% CI: 35.7–66.7%]), respectively. The results are limited by the small number of unbiased studies. Nonetheless, the age/gender prevalence differences could be used to inform future models of CE burden.

Introduction

Echinococcus granulosus is a tapeworm belonging to the family Taeniidae. This zoonotic parasite maintains itself primarily in a lifecycle between domestic dogs (definitive host) and domestic ungulates (intermediate host). Humans become infected by the accidental ingestion of E. granulosus eggs shed in the feces of infected canids, resulting in cystic echinococcosis (CE). CE is characterized by cystic lesions, most commonly in the liver and lungs, which can be fatal if not treated with surgery and/or chemotherapy.

Because of the severity of disease that can be caused by CE and its cosmopolitan distribution, CE was included in the World Health Organization (WHO) initiative to assess the global burden of foodborne diseases. As part of this initiative, the Foodborne disease burden Epidemiology Reference Group (FERG) was created as an international experts panel to gather information on the frequency of foodborne infections and their associated manifestations globally. The information reported here was contracted by the FERG to determine the status of current knowledge of the frequency and clinical manifestations of CE globally.

Materials and Methods

Search strategy and information sources.

Two systematic searches of the literature were conducted for the years 1990–2008 to gather valid information on 1) the prevalence proportion and incidence rate (IR) of CE and 2) the frequency of clinical manifestations associated with CE. PubMed, Commonwealth Agricultural Bureau (CAB) Abstracts, and 22 international databases (Table 1) were screened for articles published from January 1, 1990 to June 1, 2008. In PubMed, the search strategy included the Medical Search Heading (MeSH) terms: “echinococcosis/epidemiology” and “echinococcosis/statistics or numerical data” for the epidemiology search and the MeSH terms “echinococcosis/complications,” “echinococcosis/history,” “echinococcosis/pathology,” “echinococcosis/radiography,” “echinococcosis/radionuclide imaging,” “echinococcosis/rehabilitation,” and “echinococcosis/ultrasonography” for the search on clinical manifestations associated with CE. Because CAB Abstracts and the international search engines did not allow for searches using MeSH terms, they were queried using the following keywords: “echinococcosis,” “hidatidosis” (the Spanish spelling of the disease), and “hydatidose ou kyste hydatique” (the French spelling of the two terms used for the disease). Searches conducted in CAB Abstracts were further restricted to “humans.”

Table 1

Results of search strategies to identify articles on cystic echinococcosis epidemiology (epi) and clinical manifestations (man) published between January 1, 1990 and June 1, 2008

Database Link Hits (epi) Hits (man)
African Women's Bibliographic Database http://www.africabib.org/women.html 0 0
African Journals Online http://www.ajol.info/ 1 2
Bibliothèque Santé Tropicale http://www.santetropicale.com/resume/catalogue.asp 0 0
Bioline International http://www.bioline.org.br/journals 1 1
CAB Abstracts http://www.cabi.org/databasesearchtools.asp 470 451
CUIDEN http://www.index-f.com/ 2 0
Ecole Nationale de la Santé Publique http://www.bdsp.tm.fr 11 0
Find Articles http://www.findarticles.com/ 0 1
GreySource http://www.greynet.org/greysourceindex.html 0 0
Ind Med http://indmed.nic.in 4 23
Institute of Tropical Medicine (ITM) in Antwerp Belgium http://lib.itg.be:8000/webspirs/start.ws 1 5
IranMEDEX http://www.iranmedex.com/english/index.asp 12 16
Japan Science and Technology Information Aggregator http://www.jstage.jst.go.jp/browse/ 2 0
KoreaMed http://www.koreamed.org/SearchBasic.php 0 1
Médecine et Pharmacie de l'Université, Bamako http://www.keneya.net 0 0
MetaBase http://infolac.ucol.mx/boletin/14_1/innovaciones1.html 0 0
OpenMED@NIC http://openmed.nic.in 0 0
PUBMED http://pubmed.org 660 1,690
Science Research Portal http://scienceresearch.com/search/index.php 11 30
WHO Africa http://indexmedicus.afro.who.int/ 0 1
WHO Eastern Mediter http://www.emro.who.int/HIS/VHSL 36 141
WHO South-East Asia http://www.hellis.org 0 0
WHO Western Pacific http://www.wpro.who.int/information_sources/library_services/wprim.htm 0 2
The Trials Register of Promoting Health Interventions (TRoPHI) http://eppi.ioe.ac.uk/EPPIWeb/home.aspx?Control=Search&SearchDB=trials&page=/hp/ 0 0

Only one copy of unduplicated documents was kept for analysis. Studies were selected that included original epidemiological data on CE frequency (epidemiology search) or CE clinical manifestations (clinical manifestations search). Books and conference abstracts were excluded because they were unlikely to present original data or to have sufficient details on methods to judge the validity of the study. Dissertations, theses, and memoirs were included in the search.

Eligibility criteria.

All eligibility criteria were defined a priori. The exclusion criteria for phase I were: 1) wrong agent (for example, Echinococcus multilocularis); 2) animal data only; 3) no original data on the frequency of CE for the epidemiology search or on clinical manifestations associated with CE for the clinical manifestations search; 4) case series with < 20 participants for the clinical manifestations search and case series without an incidence rate (IR) estimate for the epidemiology search; 5) review articles without original data; and 6) editorials or letters to the editor without original data. Documents without abstracts were automatically included in the next phase. Eligible documents after phase I were obtained in full. Articles that could not be located either online or through Texas A&M University or University of Oklahoma Health Sciences Center library searches were requested through interlibrary loan or through the WHO's library. If articles could not be located by these means, an attempt was made to contact the corresponding author of the article in question. If the author could not be contacted or did not respond to the inquiry, the article was not reviewed past phase I.

Each full document was subjected to a qualitative review (phase II) and a quantitative review (phase III). The exclusion criteria for phase II included all criteria used in phase I in addition to 1) high potential for selection bias, defined as the absence of or incomplete information on the source population for the epidemiology search; 2) data not meeting the diagnostic criteria for CE; or 3) all data from before 1990. Diagnostic criteria for CE included one of the following:

  1. 1.  Typical organ lesions detected by imaging technique (for example, ultrasound, computed tomography scan, radiography, magnetic resonance imaging)
  2. 2.  Specific serum antibodies by high sensitivity serological test and confirmed by a separate high specificity serological test
  3. 3.  Histopathology or parasitology compatible with CE (for example, direct visualization of the protoscolex or hooklets in cyst fluid)
  4. 4.  Detection of pathognomic macroscopic morphology of cyst(s) in surgical specimens
  5. 5.  Detection of E. granulosus nucleic acid in a clinical specimen

Articles reviewed in full were restricted to languages that at least one member of the research team could read and understand namely English, French, Russian, Ukrainian, Chinese, Italian, Romanian, German, Spanish, and Portuguese. In addition, articles in other languages that were available in electronic format that could be translated into English using an online translator were reviewed if the translation was deemed acceptable. Studies published before 1990 were excluded because it was felt that the prevalence proportion, IR, and manifestations data would be outdated for estimating the global burden of disease between 1995 and 2005, which was the intended use of these data.

Study selection, data collection items, and data items.

The search strategy for both reviews was conducted in three phases. In phase I, all documents retrieved were screened based on title and abstract. The full reference of each article, the country where the study was conducted, the decision on inclusion for phase II, the reason for exclusion (if applicable), and the language of the document were entered into an Excel spreadsheet (Microsoft Corp., Redmond, WA). Quality assessment (phase II) and data extraction (phase III) for each document were carried out by two reviewers, when possible. All documents were reviewed by at least one senior researcher (CB or HC). Disagreements or uncertainties were resolved through discussion with other reviewers. Data were entered into standardized electronic forms of the data extraction tool that was developed in Access (Microsoft Corp.) specifically for this review (available from the authors on request). Data were collected on the study characteristics (design, geographic location, period, and duration of the study), participant selection, and ascertainment of outcome. For documents that could potentially be included in the review, but had incomplete or missing data, at least two attempts were made to contact the authors for clarification and/or additional information.

Risk of bias in individual studies.

Misclassification bias was reduced by opting not to include studies that relied solely on diagnosing patients using a single serological test. Because participants in community-based studies were rarely selected at random, it was decided to include large community-based studies of volunteers. This undoubtedly introduces a possible selection bias, the direction of which will be discussed later. In terms of hospital-based data, represented hospitals were often referral hospitals that tend to treat the sickest patients. In addition, the source and/or target populations for hospital-based studies were often estimated through the population size in the catchment area of the hospital. This necessitated relying on a calculation of surgical incidence provided by the author, the accuracy of which could not be assessed.

Risk of bias across studies.

Bias across studies was possible because most community and hospital-based studies were conducted in known high endemic areas. In addition, bias could exist because community imaging-based studies were not evenly distributed between high endemic regions caused by large multi-year research programs targeting specific locations (for example, western China) and limited availability of imaging in areas such as sub-Saharan Africa. The inclusion of CE in the list of notifiable diseases also varies across countries, which could impact awareness of the disease and, therefore, the locations where studies take place. An attempt was made to decrease publication bias by including numerous publication languages, including Chinese, Russian, French, and Spanish.

Summary measures.

For the epidemiologic review, the prevalence proportion of CE in community-based studies was estimated by dividing the number of individuals who were imaging positive, by the total number of individuals who had imaging. For hospital-based studies, the annual IR of CE hospitalizations was estimated by dividing the number of hospitalized CE cases by the reported catchment population for the hospital being studied (multiplied by the number of years of the study when appropriate). Whenever possible, these estimates were stratified by age and gender. For the review of clinical manifestations, the distribution of manifestations was reported by cyst location (hepatic or pulmonary). For each location, the proportion of each manifestation was estimated by dividing the number of cases with each manifestation by the total number of CE cases with that location.

Data synthesis and additional analysis.

Random-effect log binomial models were run to estimate the prevalence of CE in community-based studies for countries with three or more studies and for the proportion of presenting clinical manifestation for surgical hepatic and pulmonary CE cases, using the R META package (Version 0.8-2; by Guido Schwarzer in the R META metagen function) from R statistical software (R Development Core Team, www.R-project.org). Both fixed-effects and random-effects models were investigated, but given the significant variation in the estimated prevalence values, as indicated by the Q statistic, only the random-effects results are presented. The inverse variance method (Cooper H and Hedges LV) was used to pool the proportion estimates in the random-effect models and calculate the appropriate 95% confidence intervals (95% CIs).1 When available, frequency data were reported by age and sex. A Bayesian random-effect log-binomial meta-regression was fitted to estimate the prevalence proportion ratios (PPR) and their 95% Bayesian Credible Interval (95% BCI) to evaluate the effect of sex and two age groupings on CE prevalence from community-based studies.2

Results

A total of 1,211 articles were identified through the CE epidemiology search (Table 1). Of these, 528 met the inclusion criteria for phase II review, with studies of the wrong agent, review papers, and case reports being the most common reasons for exclusion. Forty-five articles had data abstracted in phase III, with no frequency data being the most common reason for exclusion. The flow diagram for the CE epidemiology search is presented in Figure 1.

Figure 1.
Figure 1.

Flow chart of cystic echinococcosis epidemiology systematic review.

Citation: The American Society of Tropical Medicine and Hygiene 88, 6; 10.4269/ajtmh.12-0692

A total of 2,366 articles were identified through the CE clinical manifestations search (Table 1). Of these, 779 met the inclusion criteria for phase II and 25 met the inclusion criteria for phase III. The most common reason for exclusion in both phase I and phase II was case reports or case series with < 20 participants. The flow diagram for the CE manifestations search is presented in Figure 2.

Figure 2.
Figure 2.

Flow chart of cystic echinococcosis clinical manifestations systematic review.

Citation: The American Society of Tropical Medicine and Hygiene 88, 6; 10.4269/ajtmh.12-0692

Community-based studies (Tables 2–5, Supplemental Table 1).

Details on source, study population, study design, and measurement are available in Table 2 for community-based ultrasound or radiological cross-sectional surveys estimating the prevalence of CE. We included 31 abdominal ultrasound-based studies that reported prevalence estimates ranging from < 1–7% in 14 countries. Three countries had at least three community-based prevalence estimates that could be combined in a meta-analysis (Figure 3AC), with resulting pooled estimates of 3.04% (95% CI: 2.05–4.23%), 1.67% (95% CI: 1.19–2.23%), and 4.82% (95% CI: 3.91–5.81%) in China, Argentina, and Peru, respectively. Four community studies were identified that focused on children, including one from Turkey and three from Argentina (Table 2)1921,23; the studies from Argentina were all from the same highly endemic area of Rio Negro Province and were the subject of the meta-analysis found in Figure 3C.

Table 2

Description of community-based cross-sectional studies reporting the prevalence of hepatic and pulmonary cystic echinococcosis based on imaging

Country (study date) Reference (language) Source population Target population *Sampling strategy CE definition Number of participants/ population (%) Prevalence of hepatic CE Prevalence of pulmonary CE Likelihood for selection bias
China (2002–2003) 3 (English) People living in Guyuan, Longde, and Xiji counties, Ningxia Hui Autonomous Region People aged 5 years and older living in these villages Volunteers/Census Abdominal ultrasound Guyuan: 983/3,990 = 25% Guyuan: 3/983 = 0.30% NA High (2 villages)
Xiji: 3,139/8,655 = 36% Xiji: 69/3,139 = 2.2%
Longde: 161/200 = 80% Longde: 1/161 = 0.62%
China (2001–2002) 4 (English) Population of eastern Xiji county, Ningxia Hui Autonomous Region People living in the village of Nanwan known for CE family cluster Census Abdominal ultrasound 113/159 = 71% 12/113 = 10.6% NA Small
China 5 (English) Population of Altai and Tacheng Prefectures, Xinjiang Uygur Autonomous Region People living in the Kekergash or Narenhebuke communities Volunteers/Census Abdominal ultrasound Tacheng: 1,844/2,631 = 70% Tacheng: 49/1,844 = 2.7% NA High (1 Prefecture)
 Altai (1990–1991) Altai: 1,861/6,424 = 29% Altai: 17/1,861 = 0.91%
 Tacheng (1995–1996)
China (2002) 6 (Chinese) Population of Habahe and Qinghe Counties, Xinjiang Uygur Autonomous Region People aged 5 years or older living in Habahe and Qinghe Counties Census Abdominal ultrasound Not available from paper Habahe: 17/889 = 1.9% NA High
Qinghe: 31/536 = 5.8%
China (1997–1998) 7 (Chinese) Population of Shiqu and Ganzi Counties, western Sichuan Province People in 4 townships from each county Random (cluster strata) Abdominal ultrasound Not available from paper Shiqu County: 60/1,249 = 4.8% NA Probably high
Ganzi County: 25/2,750 = 0.91%
China (2000–2002) 8 (English) Population of Shiqu County, western Sichuan Province People living in 26 villages of Shiqu County Volunteers Abdominal ultrasound Not available from paper 216/3,199 = 6.8% NA Probably high
China (1995–2005) 9 (Chinese) Population of Qinghai Province People living in this province Random (cluster strata) Abdominal ultrasound Not available from paper 866/2,2675 = 3.8% NA Impossible to determine
China (1997–1998) 10 (English) Population of Chindu, Zeko and Gade Counties, Qinghai Province Residents of the 3 counties where the study was advertised Volunteers Abdominal ultrasound Not available from paper 243/3,703 = 6.6% NA Probably high
China (2002) 11 (Chinese) Population of Yushu County, Qinghai Province People aged 2 years or older living in 4 villages of Yushu County Random (cluster strata) Abdominal ultrasound Not available from paper 28/1,070 = 2.6% NA Possibly small (random sampling)
Mongolia (2000) 12 (English) Population of Bulgan community, western Mongolia People living in Bulgan community Volunteers Abdominal ultrasound 1,609/6,7300 = 2.4% 4/1,609 = 0.25% NA High
Peru (2004) 13 (English) Population of Yanahuanaca district, Pasco department People older than 5 years of age living in 9 rural communities, Yanahuanaca district Volunteers Abdominal ultrasound and thoracic radiographs 949/1,836 = 52% 45/949 = 4.7% 9/829 = 1.1% High
Peru (dates not given) 14 (English) Population of Canchayllo village (Peruvian highlands) People older than 5 years of age living in Canchayllo Volunteers Abdominal ultrasound 389/1,245 = 31% 21/389 = 5.4% NA High
Peru (1994–1995) 15 (English) Population of Tupac Amaru farming cooperative (central Peruvian Andes) People older than 5 years of age living in Tupac Amaru Volunteers Abdominal ultrasound and thoracic radiographs 407/887 = 46% 15/407 = 3.7% 8/407 = 2.0% High
Peru (1997–1998) 16 (English) Population of the village of Vichaycocha People older than 5 years of age in Vichaycocha Volunteers Abdominal ultrasound and thoracic radiographs 214/517 = 41% 12/214 = 5.6% 8/214 = 3.7% High
Morocco (2000–2001) 17 (English) Population of Ifrane and Khenifra prefectures People living in Ifrane and Khenifra Volunteers Abdominal ultrasound Not available from paper (high according to personal communication with MK) Ifrane: 68/7,282 = 0.93% NA Small
Khenifra: 58/4,330 = 1.3%
Sudan (2002) 18 (English) Population of one village of Gezira state People aged 5-60 years living in the village of Um Zukra Random (specific method not provided) Abdominal ultrasound 300/4,000 = 7.5% 1/300 = 0.33% NA High
Argentina (1984–1986/1997–1998) 19 (English) Primary school-aged children living in 3 departments, Rio Negro Province Asymptomatic children (6–14 years of age) from schools in Pilcaniyeu, El Bolson, and Norquinco departments Census Abdominal ultrasound 1984–1986: 268/268 = 100% 1984–1986: 15/268 = 5.6% NA None
1997–1998: 451/451 = 100% 1997–1998: 5/451 = 1.1%
Argentina (1997–2002) 20 (English) Primary school children living in Rio Negro Province Children (6–14 years of age) attending 85 and 9 schools in 7 endemic and one non endemic department, respectively Census Abdominal ultrasound Endemic: 4,644/5,379 = 86% Endemic depts.: 70/4,644 = 1.5% NA Small
Non-endemic: 1,101/1,101 = 100% Non-endemic depts.: 0/1,101 = 0%
Argentina (1997–1998) 21 (English) Children in the town of Ingeniero Jacobacci, Rio Negro Province Children (7–14 years of age) attending all schools in Ingeniero Jacobacci Census Abdominal ultrasound 1,070/1,070 = 100% 24/1,070 = 2.2% (with additional imaging confirmation) NA None
Mexico (2002) 22 (English) Population of rural communities in the State of Mexico Individuals from the study village Random (sample of 394 households) Abdominal ultrasound Population participating over total village population: 401/1,911 = 21% 3/401 = 0.7% NA High
Turkey (dates not given) 23 (English) Children living in Manisa Province in Western Turkey Children (7–17 years of age) living in one of the three study villages Census Abdominal ultrasound Not available from paper 2/630 = 0.3% NA High
Turkey (dates not given) 24 (English) Children living in Manisa, Western Turkey Children (7–14 years of age) in 37 primary schools in Manisa Random (cluster strata) Abdominal ultrasound Population participating over total population of children in primary school 6,093/166,766 = 3.6% 9/6,093 = 0.15% NA Small (random sample)
Tunisia (dates not given) 25 (English) Population of the village of Sisseb Dar Bein Aicha People (> 5 years of age) in Sisseb Dar Bein Aicha Census Abdominal ultrasound 1,434/1,537 = 93% 50/1,434 = 3.5% NA Small
Libya (dates not given) 26 (English) Population of northwestern Libya Residents of 5 rural communities in northwestern Libya Volunteers Abdominal ultrasound Not available from paper 57/4,103 = 1.4% NA High
Libya (1994–1995) 27 (English) Population of coastal areas of Lybia Residents of 36 coastal villages Volunteers Abdominal ultrasound Not available from paper 339/20,200 = 1.7% NA High
Ethiopia (1989) 28 (English) Population of the Hamar tribal group Residents of Hamar villages in Southern Ethiopia Random (10% probability proportional sample from these hamlets) Abdominal ultrasound 990/1,060 = 93.4% 7/990 = 0.71% NA Small
Lebanon (1994–1995) 29 (English) Population of a small village in the Khums area Residents of a small village in the Khums area Volunteers Abdominal ultrasound 485/485 = 100% 22/485 = 4.5% NA None
Uruguay (1993–1994) 30 (English) Population of Florida department Residents of Florida department Volunteers Abdominal ultrasound 9,515/66,000 = 14.4% 156/9,515 = 1.6% NA High
Uruguay (1991–1992) 31 (English) Population of the village of La Paloma Residents of La Paloma Volunteers Abdominal ultrasound 1,149/1,388 = 83% 40/1,149 = 3.5% NA Small
Uzbekistan 1998 32 (Russian) Population of Uzbekistan Residents of Uzbekistan Random (Specific method not provided) Abdominal ultrasound and thoracic radiographs Not available from paper 43/7,842 = 0.55% 6/7,842 = 0.076% High
Russia (1990–1994) 33 (Russian) Population of the Stavropol administrative center Residents of Stavropol Volunteers (presumed) Abdominal ultrasound Not available from paper 73/10,606 = 0.68% NA High

Census is defined as > 70% participation.

Figure 3.
Figure 3.

(A) Abdominal ultrasound-based frequency of cystic echinococcosis in endemic areas of China (all ages) NHAR = Ningxia Hui Autonomous Region, XUAR = Xinjiang Uygur Autonomous Region. (B) Abdominal ultrasound-based frequency of cystic echinococcosis in endemic areas of Peru (all ages). (C) Abdominal ultrasound-based frequency of cystic echinococcosis in an endemic area of Argentina (school children).

Citation: The American Society of Tropical Medicine and Hygiene 88, 6; 10.4269/ajtmh.12-0692

A breakdown of available community abdominal ultrasound data by age and sex is presented in Supplemental Table 1. The meta-regression suggested that the prevalence of CE was higher in females than males (PPR: 1.35 [95% BCI: 1.16–1.53]) (Table 3). Two age breakdowns were available from community studies data (0–19, 20–39, 40+ and 0–14, 15–30, 31+), and showed that the prevalence considerably increased with age (Tables 4 and 5).

Table 3

Prevalence proportion of cystic echinococcosis cases by sex and prevalence proportion ratio (95% Bayesian Credible Intervals [95% BCI]) of the effect of being female as compared with male in community-based abdominal ultrasound studies

Country Reference Female Male Prevalence proportion ratio (95% BCI)
China 3 44/2,268 (1.9%) 31/2,505 (1.2%) 1.56 (0.99–2.47)
China 6 22/645 (3.4%) 26/780 (3.3%) 1.48 (1.28–1.71)
China 7 45/2,080 (2.2%) 40/1,919 (2.1%) 1.03 (0.68–1.58)
China 8 134/1,660 (8.1%) 82/1,539 (5.3%) 1.52 (1.16–1.98)
China 9 477/9,918 (4.8%) 296/9,103 (3.2%) 1.48 (1.28–1.71)
Peru 13 30/572 (5.2%) 15/377 (4.0%) 1.31 (0.72–2.42)
Peru 16 4.1% 6.1%
Morocco 17 75/6,864 (1.1%) 51/4,747 (1.1%) 1.02 (0.71–1.45)
Tunisia 25 34/793 (4.3%) 16/641 (2.5%) 1.72 (0.96–3.08)
Libya 26 30/2,124 (1.4%) 27/1,979 (1.4%) 1.03 (0.62–1.73)
Libya 27 211/10,356 (2.0%) 128/9,864 (1.3%) 1.57 (1.26–1.95)
Ethiopia 28 7/579 (1.2%) 1/403 (0.25%) 4.87 (0.60–39.45)
Lebanon 29 11/230 (4.8%) 11/255 (4.3%) 1.11 (0.49–2.51)
Uruguay 31 18/584 (3.1%) 22/562 (3.9%) 0.80 (0.43–1.48)
Overall estimate of prevalence proportion ratio from Bayesian log-binomial random-effect model 1.35 (1.16–1.53)
Table 4

Prevalence proportion of cystic echinococcosis by age grouping 0–19 years, 20–39 years, and 40+ years of age and prevalence proportion ratios (95% Bayesian Credible Intervals [95% BCI]) in community-based ultrasound surveys

Country Reference Age group Prevalence proportion ratio (95% BCI)
0–19 20–39 40+ 20–39 vs. 0–19 40+ vs. 0–19
China 3 1/1,750 10/774 64/2,249 22.6 (2.9–176.3) 49.8 (6.9–358.6)
China 9 94/5,486 316/6,230 340/3,777 3.0 (2.4–3.8) 5.3 (4.3–6.6)
Peru 16 1/96 3/40 8/78 7.2 (0.8–67.2) 9.9 (1.3–77.0)
Tunisia 25 9/597 11/450 30/387 1.6 (0.7–3.9) 5.1 (2.5–10.7)
Ethiopia 28 1/482 1/287 5/213 1.7 (0.1–26.7) 11.3 (1.3–96.3)
Overall estimate of prevalence proportion ratio from Bayesian log-binomial random-effect model 3.1 (1.1–10.0) 7.5 (3.2–26.4)
Table 5

Prevalence proportion of cystic echinococcosis by age grouping 0–14 years, 15–30 years, and 31+ years of age and prevalence proportion ratios (95% Bayesian Credible Intervals [95% BCI]) in community-based ultrasound surveys

Country Reference Age group Prevalence proportion ratio (95% BCI)
0–14 15–30 31+ 15–30 vs. 0–14 31+ vs. 0–14
China 10 17/1,054 79/1,178 147/1,440 4.7 (2.8–7.8) 6.7 (4.1–11.0)
Libya 26 2/1,203 6/1,205 49/1,695 3.0 (0.6–14.8) 17.4 (4.3–71.4)
Libya 27 47/8,368 111/5,754 181/6,098 3.4 (2.4–4.8) 5.3 (3.8–7.3)
Lebanon 29 7/263 8/130 7/92 2.3 (0.9–6.2) 2.9 (1.0–7.9)
Overall estimate of prevalence proportion ratio from Bayesian log-binomial random-effect model 3.3 (1.2–7.2) 6.3 (1.4–29.4)

Of the four studies conducting community surveys using portable thoracic radiographs to identify pulmonary CE cases, three were from Peru.13,15,16 In the Gavidia and others13 study, cysts were located in nine out of 829 (1.08%) study participants. Of the nine pulmonary CE patients identified, seven were female (77.8%). In the Moro and others16 study, eight out of 214 (3.74%) study participants had cysts identified on portable thoracic radiographs, with five (62.5%) being female. In the Moro and others15 study, eight out of 407 (1.97%) participants had cysts identified on thoracic radiographs. These studies were combined in a meta-analysis, with a pooled frequency of 2.06% (95% CI: 0.89–3.71%) (Figure 4).

Figure 4.
Figure 4.

Portable thoracic radiograph-based frequency of cystic echinococcosis in endemic areas of Peru.

Citation: The American Society of Tropical Medicine and Hygiene 88, 6; 10.4269/ajtmh.12-0692

Hospital-based studies (Tables 6–8).

A description of the epidemiologic characteristics of the hospital-based studies included in the systematic review of the epidemiology of CE is available in Table 6. Eleven of the 12 included studies reported an estimate of the IR from the author themselves, whereas the denominator corresponding to the population under study for one study was determined using the Food and Agriculture Organization of the United Nations (FAO) database for the corresponding years.48 Eight studies reported on surgical CE cases only, which underestimates the true frequency of cases.

Table 6

Description of hospital-based studies for cystic echinococcosis epidemiology

Country Reference (language) Region Design Diagnostic methods Source population Target population IR available (source of denominator) Number of cases reported (charts reviewed)
Egypt 34 (English) National Cohort Chart review: Imaging, serology, therapy, and histopathology or analysis of cyst fluid Catchment population of 14 generalized and specialized hospitals CE cases treated at the 14 hospitals from 1997–99 Yes (author) 133 CE cases (492,953 patients admitted)
Peru 35 (English) Chincha, Peru (185 km south of Lima) Cohort Surgical records review: Surgically confirmed CE cases Catchment population of 2 hospitals of the city of Chincha Surgical CE cases admitted at the 2 hospitals in 1996–98 Yes (author) 50 surgical CE cases (6 liver, 39 lung, 5 liver/lung)
Kyrgystan 36 (English) Bishkek, Kyrgystan Cohort Surgical records review: Surgically confirmed CE cases Catchment population of the main Bishkek surgical hospital Surgical CE cases admitted at the hospital in 1990–2000 Yes (author) 846 surgical CE cases
Palestinian Authority 37 (English) West Bank, Palestinian territory Cohort Surgical records review: Surgically confirmed CE cases Catchment population of all 7 public and 5 private hospitals on the West Bank Surgical CE cases (Palestinian) admitted in 1990–97 Yes (author) 390 surgical CE cases
Bulgaria 38 (English) National Cohort Surgical records review: Surgically confirmed CE cases Catchment population of all Bulgaria hospital surgical departments Surgical CE patients diagnosed from 1983–95 Yes (author) 3,780 CE cases
Italy 39 (English) National Cohort Chart review: In-hospital ultrasonography Catchment population of 19 Italian Echographic Departments CE patients diagnosed in 1988–90 No 424 CE cases (242,299 patients imaged)
Italy 40 (Italian) Sardigna Ecological Surveillance registry: Surgically confirmed CE cases and diagnosed non surgical CE cases Population of Sardigna Surgical and non surgical CE cases reported in 1990–91 Yes (author) 68/54 surgical CE cases
43/36 new CE cases
Morocco 41 (French) National Cross-sectional Surgically confirmed CE cases Catchment population of all provincial hospitals (Morocco population) Surgical CE cases admitted in 1992 Yes (author) 1,347 surgical CE cases
Spain 42 (Spanish) Salamanca Cross sectional Chart review: ICD-9 code 122.0 and 122.9 Catchment population of the Salamanca University Hospital (Salamanca population) CE patients treated in 1996–2003 Yes (author) 313 CE cases (252 liver, 25 lung, 21 other)
Iraq 43 (English) Arbil Province Cohort Surgical records review: Surgically and histopathologically confirmed CE cases Catchment population of the 2 main hospitals in Arbil Province CE patients diagnosed in 1990–98 No 99 surgical CE cases (4971 surgical records)
Chile 44 (Spanish) Valdivia Province Ecological Surgical records review: Surgically confirmed CE cases Catchment population of the Valdivia regional hospital (Valdivia population) Surgical CE cases admitted in 1987–91 Yes (author) 137 surgical CE cases
Turkey 45 (Turkish) National Cohort Hospital medical charts and Ministry of Health surveillance system: Surgically confirmed CE cases Population of Turkey Hospitalized cases and reported cases in 2001–05 Yes (FAO) 14,789 CE cases
Jordan 46 (English) National Cohort Surgical records review: Surgically confirmed CE cases Catchment population of major government, military and private hospitals (Jordan population) Surgical CE cases admitted in 1994–2000 Yes (author) 472 surgical CE cases
Libya 47 (English) Benghazi area of Eastern Libya Cohort Surgical records review: Surgically confirmed CE cases Catchment population of the 6 main hospitals in Benghazi (eastern Libya population) Surgical CE cases admitted from 4/91–6/02 Yes (author) 306 surgical CE cases

IRs reported from hospital-based studies (Tables 7 and 8).

We included 12 studies reporting IRs of CE by catchment population person-years. Tables 7 and 8 summarize the estimated IRs of all CE cases and of surgical CE cases, respectively. In general, National estimates of the IRs of surgical CE were lower (range of 2.3 to 5.3 surgical cases per 100,000 person-years) than studies conducted in smaller areas where the disease was known to be endemic (i.e., 32 surgical cases/100,000 person-years in the City of Chincha, Peru) (Table 8). A similar trend was observed for the estimate of the IRs of all CE cases, although only one National estimate from Turkey was available (IR = 4.4 cases/100,000 person-years) (Table 7). One study reported IR estimates from several regions of the country (Egypt), and showed a wide variation of estimates from 0 to 2.6 CE cases per 100,000 person-years.34

Table 7

Summary of incidence rate estimates of all CE cases from hospital-based studies

Country Ref Region Denominator Years Incidence rate (IR) (per 100,000 person-years)
Turkey 45 National 68,143,000 (2005 pop.) 2001–2005 4.42
Egypt 34 Giza 4,554,464–4,751,950 1997–1999 0.8–1.16
34 Matrough 2,683,728–2,800,097 1997–1999 1.34–2.6
34 Alexandria 3,515,238–3,667,662 1997–1999 0.65–0.85
34 Menoufia 194,019–202,432 1997–1999 0.27–0.83
34 Cairo 7,450,857–7,773,934 1997–1999 0.05–0.27
34 Suez 394,063–411,150 1997–1999 0.00–0.40
34 North Sinai 121,111–126,363 1997–1999 0.00–0.00
Italy 40 Sardigna 1,648,000 1990 14.9
40 Sardigna 1,648,000 1991 11.9
Spain 42 Salamanca 347,639 1996–2003 10.8
Table 8

Summary of incidence rate estimates of surgical cystic echinococcosis (CE) cases from hospital-based studies

Country Ref Region Denominator Years Incidence rate (IR) (per 100,000 person-years)
Jordan 46 National 4,827,000 (2000 pop.) 1994–2000 2.3
Bulgaria 38 National 8,357,000 (1995 pop.) 1983–1995 3.35
Morocco 41 National 25,547,000 1992 5.3
Palestine 37 West Bank 1,900,000 1995–1997 3.1
Lybia 47 Benghazi area 700,000 1991–2002 4.2
Chile 44 Province of Valdivia 259,000 1987–1991 9.1
Peru 35 City of Chincha 52,661 1996–1998 32.0
Kyrgystan 36 National 4,955,000 2000 18.0

Proportion of CE cases among different types of patients from hospital-based studies (Table 9, Supplemental Table 2).

Three studies reported on the proportion of different types of patients that were diagnosed with CE (Table 9). The estimates were extremely variable and were most likely the result of what population was chosen for the denominator rather than the true difference in the frequency of CE among countries. Available age and sex-stratified hospital-based data are available in Supplemental Table 2.

Table 9

Summary of proportion of all cystic echinococcosis (CE) cases from different populations in hospital-based studies

Country Ref Region Source Years Denominator Proportion (per 1,000)
Egypt 34 7 regions throughout Egypt 14 hospitals 1997–1999 Number of cases admitted to the hospitals 0.27
Italy 39 National 19 echographic departments 1988–1990 Number of patients imaged 1.75
Iraq 43 Arbil Province 2 major hospitals 1990–1998 Number of patients with surgeries 19.92

Distribution of manifestations of hepatic and pulmonary CE (Tables 10–12).

Table 10 summarizes the characteristics of the studies included in the systematic review on the distribution of manifestations associated with surgical hepatic CE (7 studies from 6 countries) and surgical pulmonary CE (19 studies from 6 countries). Abdominal pain was by far the most common manifestation of surgical hepatic CE, with a pooled estimate of 57.3% (95% CI: 37.3–76.1%). Presenting clinical manifestations associated with surgical cases of hepatic and pulmonary CE can be found in Tables 11 and 12. Results from random-effects models for the proportion of surgically treated hepatic CE patients that presented with abdominal pain, fever, jaundice, nausea/vomiting, and weight loss can also be found in Table 11. In addition to presenting manifestations, a pooled estimate of 27.8% (16.2–39.7%) of patients presented with an abdominal mass. This was reported in six studies and the frequency ranged between 2.4–52% of patients. Table 12 shows the results from random-effects models evaluating the distribution of various clinical manifestations associated with pulmonary CE (cough, chest pain, fever, hemoptysis, dyspnea, cyst content expectoration, and no identifiable clinical manifestations). Cough was the most common manifestation associated with pulmonary CE cases, with a pooled estimate of 51.3% (95% CI: 35.7–66.7%).

Table 10

Descriptive summary of the studies included for estimating the distribution of manifestations associated with surgical hepatic and pulmonary cystic echinococcosis (CE)

Reference (language) Country, year(s) of study Source population Target population Study sample size
49 (English) Morocco, 1990–2004 CE patients treated in Surgery Department “A” at the Ibn Sina University Hospital in Rabat 672 patients with hepatic CE 664
50 (English) Pakistan, 1986–1995 CE patients treated in Surgical Unit-I at Liaquat Medical College in Jamshoro/Hyderabad 48 patients with hepatic CE 48
51 (English) Turkey, 1991–2002 CE patients treated in the Department of General Surgery at Karadeniz Technical University in Trabzon 102 patients with hepatic CE 102
52 (English) Turkey, 1995–2005 CE patients treated at the General Surgery Clinic at Izmir Ataturk Research and Training Hospital in Izmir 73 patients with hepatic CE 73
53 (French) Algeria, Specific dates not provided CE patients operated on by the same surgical team at the surgical units of the Zeralda Hospital and the Central Clinic of Algers 100 patients with hepatic CE 100
54 (English) Jordan, 1973–1999 CE patients treated at the Department of General Surgery, Jordan University Hospital 169 patients with hepatic CE 169
55 (English) Iran, 1995–2005 Pediatric CE patients treated at the Children Medical Center Hospital in Tehran 31 patients with CE 15 (hepatic)
24 (pulmonary)
56 (English) Syria, 1993–2002 CE patients treated at the Department of Thoracic Surgery, Almouassat University Hospital Medical School, Damascus 206 patients with pulmonary CE 206
57 (English) Egypt, 1995–2004 CE patients treated at the Cardiothoracic Surgery Department, Mansoura University, Mansoura, Dakahlia 56 patients with pulmonary CE 56
58 (English) Iran, 1990–2002 CE patients treated at regional and private hospitals in Iran 120 patients with pulmonary CE 120
59 (English) Turkey, 1985–2001 CE patients treated at the Department of Thoracic Surgery, Ankara University School of Medicine, Ankara 1032 patients with pulmonary CE 1032
60 (English) Turkey, 1978–1993 CE patients treated at the Department of Thoracic and Cardiovascular Surgery, Faculty of Medicine, University of Cukurova, Adana 405 patients with pulmonary CE 405
61 (English) Turkey, 1989–1998 CE patients treated at the Department of Thoracic Surgery or the Sureyyapasa Center for Chest Diseases and Thoracic Surgery, Maltepe, Istanbul 288 patients with pulmonary CE 288
62 (English) Turkey, 1990–2005 CE patients treated at two thoracic surgery clinics in Kayseri 107 patients with pulmonary CE 107
63 (English) Turkey, 1997–2000 CE patients treated at Ataturk University, Erzurum 70 patients with pulmonary CE 70
64 (English) Turkey, 1990–2002 CE patients treated at the Thoracic Surgery Department, Dicle University School of Medicine, Diyarbakir 139 patients with pulmonary CE 139
65 (English) Libya, 1985–1991 Pediatric CE patients treated at the Al-Jala Hospital in Benghazi 43 patients with pulmonary CE 43
66 (English) Turkey, 1994–2003 Pediatric CE patients treated at two pediatric surgery clinics in Istanbul 112 patients with pulmonary CE 112
67 (English) Turkey, 1990–2001 Pediatric CE patients treated at the Department of Thoracic Surgery, Ataturk Medical Faculty, Ezurum 102 patients with pulmonary CE 102
68 (English) Turkey, Specific dates not provided Pediatric CE patients treated at the School of Medicine, Zonguldak Karaelmas University, Kozlu/Zonguldak 47 patients with pulmonary CE 47
69 (English) Turkey, 1990–2000 Pediatric CE patients treated at the Department of Thoracic Surgery, Ankara University School of Medicine, Ankara 33 patients with pulmonary CE 33
70 (French) Morocco 2002–2005 Pediatric CE patients treated at the Department of Thoracic Surgery, Military Training Hospital Mohamad-V, Rabat 23 patients with pulmonary CE 23
71 (English) Turkey 1998–2002 CE patients treated at the Department of Thoracic Surgery, Inonu University Faculty of Medicine, Turgut Ozal Medical Center, Malatya 67 patients with pulmonary CE 34 (intact cysts)
33 (complicated cysts)
72 (English) Turkey 1986–1996 Pediatric CE patients treated at the Yedikule Gogus Hastanesi Hospital in Istanbul, Turkey or the University of Vienna Medical School in Vienna 33 patients with pulmonary CE 20 (intact cysts)
14 (ruptured cysts)
(1 patient had both intact and ruptured cysts)
Table 11

Most commonly reported presenting manifestations among surgically treated cases of hepatic cystic echinococcosis*

Country Ref Total hepatic CE Abdominal pain Fever Jaundice Nausea/vomiting Weight loss Asymptomatic
Morocco 49 664 260 (39.2%) 75 (11.3%) 66 (9.9%) 59 (8.9%) 98 (14.8%)
Pakistan 50 48 14 (29.2%) 4 (8.3%) 2 (4.2%)
Turkey 51 102 80 (78.4%) 14 (13.7%) 10 (9.8%) 22 (22.0%) 12 (11.8%) 12 (11.8%)
Turkey 52 73 59 (80.8%) 7 (9.59%) 10 (13.7%)
Algeria 53 100 82 (82.0%) 20 (20.0%) 2 (2.00%) 11 (11.0%)
Jordan 54 169 50 (29.6%) 28 (16.6%) 27 (16.0%) 11 (6.5%)
Iran 55 15 10 (66.7%) 15 (100%) 4 (26.7%) 9 (60.0%)
Proportion (95% CI) 57.3% (37.3–76.1%) 14.1% (10.7–17.9%) 9.4% (5.7–14.0%) 15.6% (9.9–22.4%) 8.6% (6.7–10.6%)

Other clinical manifestations included pulmonary symptoms, urticaria, cholangitis, hematemesis, and back pain.

Pediatric cases only.

Excluding reports of only pediatric cases and estimated for manifestations reported by at least three articles.

Table 12

Most commonly reported presenting manifestations among cases of pulmonary cystic echinococcosis treated in hospitals*

Country Ref Total pulmonary CE Cough Chest pain Fever Hemoptysis Dyspnea Cyst content expectoration Asymptomatic
Syria 56 206 112 (54.4%) 75 (36.4%) 39 (18.9%) 52 (25.2%) 21 (10.2%)
Egypt 57 56 19 (17.8%) 16 (28.6%) 6 (10.7%) 12 (21.4%) 15 (26.8%) 3 (5.4%) 4 (7.1%)
Iran 58 120 75 (62.5%) 10 (8.3%) 20 (16.7%) 10 (8.3%) 5 (4.2%)
Turkey 59 1032 846 (82.0%) 629 (60.9%) 124 (12.0%) 217 (21.0%) 258 (25.0%) 155 (15.0%) 165 (16.0%)
Turkey 60 405 101 (24.9%) 208 (51.3%) 8 (2.0%) 1 (0.2%) 65 (16.0%)
Turkey 61 288 155 (53.8%) 142 (49.3%) 40 (13.9%) 61 (21.2%) 29 (10.1%) 14 (4.9%) 30 (10.4%)
Turkey 62 107 43 (40.2%) 30 (28.0%) 16 (14.9%) 2 (1.9%) 8 (7.5%) 22 (20.6%)
Turkey 63 70 38 (54.3%) 33 (47.1%) 22 (31.4%) 21 (30.0%) 11 (15.7%)
Turkey 64 139 68 (48.9%) 48 (34.5%) 39 (28.0%) 11 (7.91%) 18 (12.9%)
Iran 55 24 (ped) 22 (91.7%) 10 (41.7%) 20 (83.3%) 2 (8.3%) 11 (45.8%)
Libya 65 43 (ped) 30 (69.8%) 2 (4.7%) 16 (37.2%) 9 (20.9%) 2 (4.7%)
Turkey 66 112 (ped) 79 (70.5%) 27 (24.1%) 38 (33.9%) 2 (1.8%) 2 (1.8%)
Turkey 67 102 (ped) 57 (55.9%) 41 (40.2%) 19 (18.6%) 9 (8.8%) 21 (20.6%) 8 (7.8%)
Turkey 68 47 (ped) 35 (74.5%) 17 (36.2%) 21 (44.7%) 2 (4.3%)
Turkey 69 33 (ped) 22 (66.7%) 11 (33.3%) 6 (18.2%) 10 (30.3%) 4 (12.1%)
Morocco 70 23 (ped) 20 (86.9%) 5 (21.7%) 2 (8.7%) 2 (8.7%)
Turkey 71 34 (intact) 9 (26.5%) 17 (50.0%) 4 (11.8%) 2 (5.9%) 6 (17.6%) 9 (26.5%)
Turkey 71 33 (ruptured) 15 (45.4%) 16 (48.5%) 12 (36.4%) 11 (3.3%) 14 (42.4%) 5 (15.1%) 1 (3.0%)
Turkey 72 20 (intact-ped) 13 (65.0%) 10 (50.0%) 7 (35.0%) 2 (10.0%) 8 (40.0%) 1 (5.0%) 1 (5.0%)
Turkey 72 14 (ruptured-ped) 14 (100%) 8 (57.1%) 7 (50.0%) 8 (57.1%) 3 (21.4%) 8 (57.1%)
Proportion (95% CI) - All ages 51.3% (35.8–66.7%) 39.9% (29.8–50.4%) 14.8% (9.3–21.3%) 12.6% (5.6–21.8%) 23.7% (17.1–31.0%) 8.8% (5.1–13.3%) 12.8% (9.8–16.0%)
Proportion (95% CI) - Pediatric cases only 70.3% (61.2–78.6%) 36.5% (21.4–53.1%) 38.1% (23.4–54.0%) 12.3% (5.5–21.3%) 24.1% (9.5–42.7%) 10.2% (4.9–17.3%)

Other clinical manifestations included tachypnea, sweating, infectious symptoms, pleuritis, pneumothorax, weight loss, purulent sputum, allergic reactions, malaise, nausea and vomiting, abdominal pain, and headache.

Not included in meta-analysis.

Discussion

This is the first systematic review looking at both the epidemiology and clinical manifestations associated with CE, taking into account study type. Results from community-based studies suggest that the prevalence of CE in endemic areas is < 10% and > 1%. Although this remains a large range of values, it indicates that this disease is relatively common in the areas studied. These estimates are only available from a small number of regions, thought to be endemic, which limits our ability to extrapolate the results to a global estimate of the prevalence of CE. This is particularly true for the poorest areas of the world that do not have the funds or access to the technology for field diagnosis of CE.

Another limitation of the available literature is that several studies were conducted among volunteers, which could bias the prevalence estimates in either direction. A meta-regression analysis run on six studies of volunteers in China where participation proportion was available (data not shown) showed that, although not statistically significant, the prevalence of infection tended to increase with participation proportion. This suggests that those with undiagnosed infection may feel too sick to attend community screenings and, therefore, may suffer from some disability. This is in agreement with a study conducted in western China, which showed that the quality of life of CE cases detected through ultrasound was lower than that of individuals without CE.73 Hence, the relatively high prevalence of CE in combination with its associated disability would be important to consider in future global burden of disease assessments.

Our meta-regression of community-based surveys showed that females had a greater prevalence of infection than males. This may be caused by gender roles in endemic regions, which result in women more often taking care of the daily needs of dogs, tending gardens, and preparing food. In almost all community-based ultrasound studies, CE prevalence increased with age, which would be expected with a chronic infection such as CE. These data could be used in future studies to predict, with some uncertainty, the prevalence of CE in the regions where CE is known to be endemic.

Hospital-reported data have been largely used to estimate the IR of either surgical or symptomatic CE cases. These studies result in estimates of CE much lower than that found in community-based surveys, with IR values being about 1,000 times less than the prevalence values. If we assume that the average duration of CE from the asymptomatic phase to the symptomatic phase is about 10 years, the hospital-based studies result in estimates 100 times lower than that seen from community-based studies. This is to be expected because only a small proportion of patients will develop symptoms that are severe enough to seek medical attention and will have resources to pay for treatment. Studies using a smaller catchment population estimate as the denominator tended to result in larger estimates of IRs. This may reflect a more accurate estimate from smaller studies or, on the contrary, an underestimation of the size of the catchment population. As more community-based ultrasound and hospital-based IR data become available, models could be developed from areas where both types of estimates are available to predict the frequency of CE. The gender distribution of hospital cases were similar to that found in community-based studies. This suggests the absence of a gender bias in seeking medical care for CE. Therefore, the overall estimates of the PPRs from the Bayesian log-binomial random-effect models for distribution of community CE cases by sex should be appropriate to use with hospital-based data.

In contrast to what was seen in community-based prevalence surveys, data from hospital studies indicated that young adults and middle-aged individuals made up the largest proportion of surgical cases. Two possible reasons could lead to this observation. First, older individuals diagnosed in community studies have been infected for a long period of time, but did not develop significant clinical manifestations. Second, older patients may be less likely to seek medical attention because they may not work anymore and may not be as affected by the symptoms.

Abdominal pain was the most commonly reported presenting complaint for hepatic CE and cough the most commonly reported presenting complaint for pulmonary CE. Those manifestations would be associated with only small disability weights, further emphasizing the need for more representative studies of undiagnosed cases and their level of disability.

In conclusion, this is the first systematic review of both CE epidemiology and clinical manifestations. Although the unequal distribution of the origin of published literature and poor official reporting are acknowledged, the data obtained through this review can be used to inform and improve upon models assessing the global burden of CE.

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