Echinococcosis or hydatid disease is a near-cosmopolitan parasitic zoonosis caused by the larval stages of cestodes of the genus Echinococcus, whose spectrum of clinical manifestations can vary from asymptomatic infection to death, the liver being the most frequently affected organ. In the absence of an adequate treatment, case fatality rate of affected patients may reach 100%, so clinical suspicion should always be accompanied by a complete workup and a prompt treatment. Like other zoonotic parasitic diseases, echinococcosis is associated with low socioeconomic and cultural levels, especially affecting rural areas of developing countries, not only by the morbidity and mortality it produces, but also by the economic impact associated to health care costs and productivity losses. Despite this, in Colombia and in other South American countries, epidemiological studies of this disease are limited, so it is not known with certainty the incidence, the prevalence, and the burden of the disease. The objective of this chapter is to summarize and describe epidemiological and clinical updated aspects of the disease, focusing on evidences and published research articles on echinococcosis in Colombia, finally questioning if this cestode zoonotic disease has been largely neglected.
- neglected diseases
- zoonotic infectious diseases
Echinococcosis or hydatid disease is a near-cosmopolitan parasitic zoonosis caused by the larval stages (paratenic for humans) of cestodes of the genus
Biologically and taxonomically, although in the past it was considered as part of the genus
Although, 12 species have been recognized, only four are of public health concern and produce human pathology:
Living or having lived in rural areas where farming and animal husbandry are common is an important risk factor for this disease, in some areas particularly where people frequently come in contact with dogs that accompany paca hunters as well as where wild animal hunting for food is common practice (e.g., hunters and aboriginal people) . In addition, new population migration patterns over the past four decades have caused a change in the profile of this disease, allowing its worldwide distribution . In addition, in general, now it is considered that there is a risk of getting echinococcosis infection, as well other cestodiasis, while traveling to endemic zones.
This disease is related with extensive livestock or poor health infrastructures; usually associated with a low socioeconomic level and lack of education. Its public health importance is related not only to the high fatality rate in humans but also with reduced work performance, costs of hospitalization, interventions, and disabilities .
Although echinococcosis has been recognized for centuries (at the 17th century, Francesco Redi illustrated that the hydatid cysts of echinococcosis were of “animal” origin), in some countries of the neotropic region, such as Colombia, this disease was discovered during 20th century). Studies in this context in this country, as well as in other countries of South America, are still limited. Therefore, the objective of this chapter is to summarize and describe epidemiological and clinical updated aspects of this disease, focusing on evidences and published research articles on echinococcosis in Colombia, finally questioning if this cestode zoonotic disease has been largely neglected [1-84].
2. Organisms causing human disease
It is endemic in North America, Alaska, Europe, Central Russia, China, Turkey, Japan, Uruguay, and Argentina. In humans, the most frequently affected organs are the liver (80%), lungs (10%), brain (5%), and other organs such as kidney and pancreas (5%) .
The results of a survey (carried out to detect
Other species in the genus
Some authors have recently exposed that all these species would be infectious for humans, probably with the exception of
More importantly, a draft genomic sequence for
3. Life cycle
In these organs, the oncosphere develops into a cyst that enlarges gradually, producing protoscolices and daughter cysts that fill the cyst interior (Figure 2). The definitive host becomes infected by ingesting the cyst-containing organs of the infected intermediate host (Figure 2). After ingestion, the protoscolices evaginate, attach to the intestinal mucosa, and develop into adult stages in approximately 32 to 80 days (Figure 2). Humans can also get infected by ingesting eggs from feces of definitive hosts infected, then resulting with the release of oncospheres in the intestine and the development of cysts in different organs (mainly liver and lungs) (Figure 2).
The same life cycle occurs with
4. Geographical distribution
Cystic echinococcosis or cystic hydatidosis (caused by
In South America, although there is underreporting, it has been estimated that each year there would be occurring 2,000 cases , but these are not the exact figures. Uruguay has reported 9.2 cases per 100,000 population in 1995, and Chile has reported between 6.6 and 8.4 new cases per 100,000 population per year. Besides this, echinococcosis is also a health problem in Argentina, Bolivia, Brazil, and Peru [10, 82]. In the Peruvian Andes, observed prevalence rates in one study among humans, canines, and sheep were 9%, 46%, and 32%, respectively .
World Health Organization (WHO) had developed a global map of the distribution of
Since definitive host of
Normally, infections from species of the genus
5. Echinococcosis studies in Colombia
In Colombia, echinococcosis does not seem to be a major problem if we base such assumptions from human and animal health authorities . But, as has been evidenced, cases of infection with the larval forms of
The first case was reported in 1941 , but since 1957, more cases had been reported  (Figure 6). Two decades later, D’Alessandro began studies in the country. This author found more than a dozen of human cases of polycystic echinococcosis produced by the larval stage of
Most of the infected people were native from Colombia who acquired the disease by ingesting food or water contaminated with dog feces and by eating raw viscera of “guagua.” Botero et al. describe three more unpublished cases: two from the coast of the Pacific Ocean and one from Santa Marta [13, 14]. D’Alessandro’s studies demonstrated that in Colombia, the guagua is the main intermediate host and the wild dogs known as gouache fox is the definitive host. The guatin, which is also an edible animal for Colombian indigenous tribes, is a more specific host for
Till 2008, the country in South America with the highest number of cases reported was Brazil, with 99 cases, followed by Colombia with 29 (Figure 6) [3, 50-60]. In Colombia, some authors believe that there are more cases not reported, in fact due to the lack of records. This also probes that occurrence of echinococcosis is more evidently reported, when people in the rural and jungle areas receive health services and physicians are more aware of the disease .
Two years later, in 2010, another and the last case till March 2015, has been reported . A case of cardiac echinococcosis, detected in echocardiographic finding in an 18-year-old woman diagnosed in Medellin, Antioquia . Fortunately in this case, physicians suspected of this cestode infection; however, more awareness among physicians regarding the compromise of cardiovascular system in many parasitic diseases is still necessary, particularly in endemic areas [63-67].
Based on this review of cases, including information from the departments of the country where this disease has been reported, a map for Colombia has been proposed (Figure 6). This map shows the departments of the country (including locations of origin of one or more cases), where echinococcosis have been reported (Figure 6). At least 10 departments (out of 32 in total) have reported cases of echinococcosis (Figure 6) [14, 54, 59-61, 72].
Beyond this, with an increasing number of published reports concerning this disease, medical personnel in tropical areas, as in Colombia and more recently in Brazil, have been keenly interested in undertaking epidemiological surveys [3, 68, 69]. Even more, there is a significant zoonotic potential, given the fact that the investigations in Colombia demonstrated a large enzootic areas of transmission in the oriental plains of that country [3, 58], where multiple species and a high number of animals have been found positive in the evaluations for
As in other zoonotic diseases, parasitic and of other etiologies, there is a clear need of more studies, as well as more interaction between physicians and veterinarians. More research is necessary; currently, there are just 10 reports available in Medline for Colombia (using the terms “Colombia” AND “Echinococc*” [means
Finally, an undergoing research of our group is analyzing a new source of information for communicable diseases, which are not under surveillance and require compulsory notification. In Colombia, there is a service, which is now available for analyses, the so-called personal health records (
Although these cases corresponded in 18.2% to “Echinococcosis, unspecified, of liver” (B67.8) and 21.5% to “Echinococcosis, other and unspecified” (B67.9), there are 60.4% (n = 183) of them classified as infection due to
In these cases, looked retrospectively, the limitation in the approach is that there is no information regarding the diagnostic techniques implemented in each case, and how these cases were therapeutically managed. Then, based on this information, cross-sectional and prospective studies should be implemented in the countries, and there should also be an increase in the awareness about the existence and occurrence of such diseases in different areas of the country, and particularly in those that had previously reported case reports and case series since early decades (Figure 6).
6. Economic burden of echinococcosis
According to the World Bank, economic losses due to this disease stand at the fourth position after other diseases and trauma .
Echinococcosis also affects the economy of the endemic regions. In humans, losses are due to costs of hospitalization, treatment, disability, etc. However, in livestock, losses are due to lost productivity, losses in quality of the wool and meat, and decreased milk production and fertility . Estimated annual economic losses in Peru are $ 178,705 . In Colombia, estimation of the economic burden of this disease has not been reported, but given the increase in the number of economic evaluations of infectious diseases in the country and in the region [73, 74], there would be more clear details once the number of cases reported would be defined.
7. Clinical manifestations
Regardless of the etiology, a new concept of organ compromise was proposed in 2014, when two or more organs are affected by echinococcosis at the same time in a patient. This has been defined as multivisceral echinococcosis, simultaneous localization of hydatid cysts in more than one organ . Multivisceral echinococcosis should be differentiated from multiple echinococcosis . The latter is the localization of multiple cysts in one organ . Even in paired organs (lungs, kidneys) if both are compromised, it will be a case of multivisceral echinococcosis, given the implications not just in diagnosis, but particularly in surgical management.
Echinococcosis is a larval infection caused in humans by
7.1.1. Cystic echinococcosis
As a general rule, the phase of primary infection is always asymptomatic because the cysts are located in different organs, characterized by their small size, which is less than 5 cm and are encapsulated. This first phase is not been associated with major pathology and might remain asymptomatic for a long period or permanently [16, 17]. The incubation period is undefined but it could be in around months or even years, before the infection becomes symptomatic. There have been reported cases of spontaneous cure due to cyst calcification and collapse and on the other hand, there are cases of early symptomatology because of cyst rupture [16, 18].
7.1.2. Patient characteristics
Cystic echinococcosis is seen in all ages, including patients aged below 1 year and above 75 years, with a majority between 6 and 15 years, 21 and 30, and 30 and 40 years. The most risky profession involves farm labors .
There is a huge spectrum of clinical manifestations that are variable among the patients and none of these are considered as pathognomonic of echinococcosis . All the symptoms might depend on different characteristics such as the host-parasite interaction, the different organs involved, cyst size, and the presence of different complications such as cyst rupture or trauma [16, 18]. The most commonly compromised organs are the liver, followed by lung, kidney, spleen, and less common organs like muscles, skin, abdominal cavity, and pelvic cavity. The symptoms may vary in accordance with the organ involved [16-18].
Liver infections include symptoms such as hepatomegaly, cholecystitis, jaundice, liver abscess, or secondary biliary cirrhosis. Lung infections include symptoms like chest pain, expectoration, hemoptysis, and dyspnea . Other severe manifestations include cyst getting rupture into biliary tree causing biliary colic, jaundice and can be confused with pancreatitis or cholangitis [16, 19].
7.1.4. Liver involvement
The liver is the most commonly involved organ, representing around two-thirds of the cases. The right lobe is compromised in the majority of the cases (60% to 80%) but it frequently does not produce symptoms and when these once occur, it is estimated that the cyst size is around 10 cm [20, 21]. Once a cyst develops a larger size, hepatomegaly might occur and other symptoms like right upper quadrant pain, nausea, and vomiting can also result. Due to the mass defect of the cyst compression of the portal and hepatic veins, it can result in Budd-Chiari syndrome [19, 20].
7.1.5. Lung involvement
The most common symptom of lung infection is the presence of cough in around 53% to 62% of the patients, followed by chest pain, dyspnea, and hemoptysis. But generally, most of the patients with lung infection are asymptomatic [21, 22].
7.1.6. Other organs
Heart infection might generate rupture with pericardial tamponade, cardiac insufficiency, embolism or pericardial effusion [23-25, 60, 64, 66]. The central nervous system can lead to seizures or symptoms due to an increase in the intracranial pressure . Kidney disease can cause hematuria, and even glomerulonephritis and nephrotic syndrome have been described. Bones are mostly asymptomatic and only develop manifestations when a pathological fracture occurs .
Surgeries are performed in around 15% of the patients after the initial diagnosis. And in patients without surgery, majority would remain asymptomatic through many years .
The most common presenting complaints include malaise, weight loss, and right upper quadrant discomfort due to hepatomegaly. Cholestatic jaundice, cholangitis, portal hypertension, and the Budd-Chiari syndrome can also occur. The clinical presentation may mimic that of hepatocellular carcinoma .
Extrahepatic primary disease is very rare (1% of cases). Multiorgan disease was described in 13% of cases in one series in which metacestodes involved the lungs, spleen, or brain in addition to the liver . If left untreated, more than 90% of patients will die within 10 years of the onset of clinical symptoms, and virtually 100% will die by 15 years .
For an optimal diagnosis, both imaging and serological tests are required.
The cysts may be visualized by ultrasonography, computed tomography (CT), or magnetic resonance imaging (MRI). However ultrasonography is the most commonly employed technique due to its easy performance and low cost. The sensitivity of ultrasonography for the evaluation of echinococcosis is 90% to 95% and the appearance of a cyst in the ultrasound is as an anechoic and smooth cyst. Another important aspect of the ultrasonography is that it helps in the classification of the disease, according to the WHO echinococcosis classification based on their ultrasound appearance. CT has an overall sensitivity of 95% to 100% and is the preferred imaging test to describe the size, location, and number of cysts. MRI has the same sensitivity as that of CT and has no major advantages over CT, but it is better for the determination of intra- and extra-hepatic changes; however, it is not usually a routine examination technique in the patients [18, 27].
8.2. Serological tests
They are used in the diagnosis and follow-up of the patients. Some of the laboratory tests include complement fixation, latex agglutination, and indirect immunofluorescence [27, 84]. However, there are two important antigens of the
8.3. Other laboratory tests for diagnosis
Nonspecific leukopenia or thrombocytopenia, mild eosinophilia, and nonspecific liver function may be detected but are not diagnostic. Hypergammaglobulinemia and elevated serum IgE levels are present in more than 50% of cases.
Imaging: On ultrasonography or CT, the lesions usually have an irregular contour with no well-defined wall, central necrosis, and irregular intralesional and wall calcifications.
8.4. Comparing serologies
Serologic tests are more reliable for diagnosis of
Cyst aspiration or biopsy: In the absence of a positive serologic test, percutaneous aspiration or biopsy may be required to confirm the diagnosis by demonstrating the presence of protoscolices, hooklets, or hydatid membranes.
Polymerase chain reaction: Polymerase chain reaction techniques are limited to research settings but may play a diagnostic role in the future. DNA probes using Southern hybridization tests are also being developed.
Echinococcosis treatment includes a multidisciplinary conduct and a general overview of the patient condition in order to provide the best management that includes surgical treatment, pharmacological treatment, the “watch and wait,” and both of them, depending on the specific characteristics of the disease and most importantly the type of Echinococcosis that the patient develops. The overall approach depends on the different species that infect humans, particularly two of them:
9.1. Cystic echinococcosis
As mentioned earlier, the treatment is complex, and even these days there are no clinical trials and studies that compare the different modalities to say which one is superior to the other. However, it is accepted that the surgical treatment can potentially remove all the
Overall, the diagnosis approach depends on the WHO diagnostic classification, performed in 2003, when the Informal Working Group on echinococcosis established a standardized ultrasound classification based on the status of the cyst by its ultrasound appearance. This classification has the intention to promote uniform standards of diagnosis and treatment, and has important implications for the clinical decision.
There are three different stages, including CE1 and CE2 that are cyst-containing protoscolices. The CE3 stage is divided in CE3a, a detached endocyst, and CE3b, a solid cyst with daughter cysts . Recommendations indicate that CE1 and CE3a stages, in which the cyst size is less than 5 cm, should be treated with albendazole only. Stages CE1 and CE3a with cyst size more than 5 cm may be treated with albendazole in combination with percutaneous treatment via PAIR (puncture, aspiration, injection, and reaspiration). The CE2 and CE3b stages are characterized by multiple cyst compartments that require individual puncture, and these patients usually require PAIR. However, the optimal choice among the different approaches (PAIR, surgery, or drug therapy) is uncertain. Finally, stages CE4 and CE5 involve inactive cysts that only require observation [33, 34].
9.2. Treatment options
It is the first treatment option in cases of complicated cysts, including a cyst rupture or infection and hemorrhage. It is also an alternative treatment option for those cysts with many daughter vesicles that are not suitable for percutaneous treatment. Another indications are large liver cysts, cyst diameter more than 10cm, extrahepatic disease (lung, bone, or brain), cysts situated superficially with high risk of rupture, and cysts affecting the biliary tree [31, 35]. Contraindications are relative to each patient; for example, old-aged people, people suffering from concomitant diseases, pregnant women, or patients with small cysts . As far as the complications are concerned, secondary infection, intra-abdominal abscess, fistula, or sclerosing cholangitis have been reported. Recurrent echinococcosis may occur in e 2% to 25% of the cases, depending basically on the surgeon’s experience .
Before choosing the surgical technique, it's important to administrate drug therapy to minimize the surgical risk of secondary echinococcosis from seeding of protoscolices in the abdominal cavity. Usually, albendazole is administered a week before surgery, and continued at least four weeks after the surgery. Praziquantel is another option, but there is no specific evidence regarding its efficacy [31, 36].
Surgical approach must be individualized, depending on each patient disease and its characteristics. There are two options; the first one is to remove the intact cyst, and another option is to open the cyst with protoscolicidal agents, such as hypertonic saline, followed by the evacuation of the cyst contents and removal of the cyst . Other protoscolicidal used includes 70% to 95% ethanol and 0.5% cetrimide solution. The protoscolicidal agent must be in contact with the germinal layer for at least 15 minutes to make its effect. Albendazole, ivermectin, and praziquantel have been also used as protoscolicidal agents, but their efficacy and safety need more studies. Protoscolicidal agents should not be used in the presence of biliary communication, because of the risk of sclerosing cholangitis or pancreatitis [31, 35].
There is also the possibility of laparoscopic surgery for the treatment of echinococcosis; however, there are no randomized trials done yet comparing the efficacy of laparoscopy with open procedures. Possible indications for laparoscopic treatment are the presence of anteriorly located hepatic cysts, although this procedure is related with associated risk of spillage because of the elevation of intra-abdominal pressures due to the pneumoperitoneum. Contraindications include deep intraparenchymal cysts, the presence of calcified walls cyst, and cysts located next to the vena cava .
In a review article published in 2014 with the aim to study the world literature of the laparoscopic treatment of liver hydatid cyst, a total of 914 patients were identified to evaluate the mortality, morbidity, and clinical outcomes of the laparoscopic treatment. It was found that the most common procedure was cystectomy in 60.39% of patients, followed by partial pericystectomy with 14.77% of patients, and finally pericystectomy with 8.21% of patients, and the rest of them were treated via segmentectomy. They also reported that conversion of laparoscopy to open laparotomy occurred in the 4.92% of the cases, due to anatomical limitations and inaccessible locations. Mortality was reported in 0.22% of the patients and morbidity was reported in 15.07% of the patients. There was no intraoperative deaths reported and the most reported complication was bile leakage. In general terms, they concluded that the laparoscopic procedure is safe, with acceptable ranges of mortality and morbidity and clinical outcomes comparable to open surgery .
9.2.2. Percutaneous management
There are two percutaneous techniques. The first one called PAIR (puncture, aspiration, injection of a protoscolicidal agent, and reaspiration) is usually effective in the treatment of cysts without daughter cysts. And the second one, that involves the evacuation of the cyst with a large bore catheter. This technique helps in cases in which the drain becomes difficult or tends to relapse after PAIR, like in the case of WHO stages CE2 and CE3b cysts [31, 38]. Percutaneous treatment is associated with anaphylaxis, happening according to a review in the 1.6% of the patients . And as in surgery, albendazole must be administered for at least one month after the percutaneous treatment .
9.2.3. PAIR procedure
It was first introduced in the mid-1980s and includes the realization of percutaneous puncture of the cyst by ultrasonic guidance, aspiration of the cyst fluid, injection of a protoscolicidal substance, and finally reaspiration of the cyst fluid. PAIR has the advantages of being less invasive than surgery and can be a diagnostic and therapeutic procedure and it has a success rate of more than 95%. This procedure may be used in cases of echinococcosis of WHO stages CE1 and CE3a as primary treatment and for the relapse after medical therapy in stages CE1 and CE3a, and in case of relapse after surgery. PAIR also showed to be successful in the management of liver cysts and in those cysts located in other abdominal parts such as kidney, spleen, and in the abdominal cavity. There are controversies in the use of PAIR in pregnant women and in children, although the application of PAIR is indicated in symptomatic pregnant women [16, 31, 38].
The procedure is performed by ultrasound or by CT guidance. Then the cyst is punctured and the fluid aspiration is realized and a histopathological study must be done to evaluate the presence of protoscolices. After the administration of protoscolicidal agent, the reaspiration must be done for at least 10 to 15 minutes. Four hours before PAIR, adjunctive drug therapy with albendazole or mebendazole should be administrated. Recommendations indicate that albendazole should be continued after a month of the procedure and mebendazole should be continued for three months. The most important contraindications of the PAIR are the following: the presence of cysts without drainable solid material, superficial cyst with risk of rupture in the abdominal cavity, calcified cysts, and cyst with biliary communication [31, 40].
9.2.4. Drug therapy
In most of the cases, it is useful as an adjunctive therapy to surgery and percutaneous treatment. The use of pharmacological approach as definitive management is indicated in few cases. The recommendations indicate that in cases of small cysts of WHO stages CE1 and CE3a with cyst size less than 5 cm, the initial management with only drug therapy is appropriate, with optimal duration of treatment depending on the clinical factors, but usually estimated in around one to six months. The effectiveness of pharmacological therapy decreases with the presence of a cyst size more than 5 cm, with multiple compartments of cysts [16, 31, 39].
As an adjunctive treatment, albendazole is used as perioperative drug therapy in surgery or in percutaneous treatment. It reduces the risk of recurrent disease by the inactivation of the protoscolices. There is no general consensus of the duration of the treatment, but generally it is initiated four days before surgery and continued at least one month after the surgery in case of albendazole and for three months in case of mebendazole [16, 31, 40, 42].
Albendazole is the first drug option and the primary antiparasitic agent for treatment of
However, albendazole has more advantages than mebendazole. For example, albendazole is well tolerated by patients and it takes a shorter duration of therapy. Dose of albendazole is usually 10 to 15 mg/kg per day divided in two doses and mebendazole dose is 40 to 50 mg/kg per day divided in three doses. Adverse effects include hepatotoxicity in 1% to 5% of the patients, cytopenia, and alopecia in less than 1% of the patients. Due to hepatotoxicity, there might be an increase in aminotransferase enzymes. Other rare side effect like agranulocytosis has also been reported. Contraindications of using albendazole include patients with liver disease or bone marrow suppression [31, 44]. Patients with pharmacological therapy must be monitored every two to three weeks for first three months and then monthly . Praziquantel has protoscolicidal activity, but its efficacy in clinical studies is variable, but is considered as an alternative when the albendazole treatment cannot be administrated [44, 45].
Observation: Also known as the “watch and wait,” indicated in the WHO stages CE4 and CE5, in patients with absence of complications or inactive liver cysts .
9.3. Alverolar echinococcosis
Unfortunately, the treatment of alveolar echinococcosis is less effective than the treatment of cystic echinococcosis. The general approach to the treatment is based on surgery. The main idea is to remove all the infected tissue and sometimes it is necessary to also remove part of the host tissue. Management with albendazole is recommended after surgery with an uncertain optimal duration. The benefit of preoperative albendazole administration has not been reported .
Echinococcosis has always been neglected worldwide and especially in Colombia. Particularly in this country, research was done and published only between 1950s and 1990s. There is no subsequent interest in the occurrence of this disease and all its implications.
Due to the impact of echinococcosis, the burden it creates, and the consequences in the patients, it becomes important to create strategies in order to improve and have a better control on this disease in our country. This probably should begin at medical schools, where more emphasis on teaching about this parasitic disease, would increase awareness about it. As has been mentioned earlier, there should be regular interaction among physicians, biologists and veterinarians to better understand the implications of this zoonotic disease, which at least from an enzootic point of view is clearly extended. As an additional reflection in the middle of the process and discussion about peace in Colombia, there are chances that once this would be reached, after the La Habana discussions, more people, not only missionary, health, and military corps, would be allowed to enter in the guerrillas-controlled areas, which are precisely located where enzootic evidences of echinococcosis have been reported, increasing the exposure to species of
Even more, it’s not clear yet, if Colombia would be considered properly a risky area for travelers visiting the country in the view of acquisition of echinococcosis. But certainly in other highly endemic countries, echinococcosis is included in the list of infectious diseases that can be acquired during travel, and cases of echinococcosis, as well from other cestodiasis, have been reported increasingly during the last few years [75-78].
Therefore, it becomes crucial to create a clear and easy consensus to help and guide the physicians to make a better approach towards helping the patients in finding the opportune diagnosis and the best treatment option. The creation of a normative and the global vision of echinococcosis as a public health problem might help improve the control of this disease.
Echinococcosis, and other zoonotic diseases, can re-emerge just when they are considered to be under control or eliminated. They can go into hiding in the animal reservoirs, so there is no possibility for complacency . Epidemiology of zoonoses such as echinococcosis is complex and dynamic, being influenced by varying parameters that can roughly be categorized as human-related, pathogen-related, and climate/environment-related [79, 80]. But certainly for echinococcosis, there is still much to understand.
Authors would like to thank the critical comments of anonymous reviewers. Also, Dr. Rodriguez-Morales would like to thank Dr. Juliana Buitrago-Jaramillo, Dean, Faculty of Health Sciences, Universidad Tecnológica de Pereira, Pereira, Risaralda, Colombia, for her support to his research group during the activities in year 2014, including presentation and conferences at major international meetings (mainly in Peru, Mexico, and Cuba), and also in 2015 (Ecuador). The authors would also like to thank the Asociación Colombiana de Infectología and International Society for Chemotherapy, for supporting the research and presentations of studies in zoonoses since 2011 (Italy, Japan, Brazil, Ecuador, Mexico, Peru, Cuba). Finally, the authors would like to thank the Ministry of Health of Colombia, for the access to SIVIGILA and RIPS databases through the system Cubo de datos del SISPRO.
Moro P, Schantz P. Echinococcosis: A review. Int J Infect Dis. 2009;13: 125-133.
McManus D, Zhang W, Li J, Bartley P. Echinococcosis. Lancet. 2003;362:1295-1304.
D’Alessandro A, Rausch RL. New aspects of neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin Microbiol Rev. 2008;21(2):380-401.
Khanfar N. Hydatid disease: A review and update. Curr Anaesth & Crit Care. 2004;15:173-183.
Soledad S, Rodríguez V, Candia M, Bonastre P. Hidatidosis Pulmonar. Revista de Posgrado de la VIa Cátedra de Medicina. 2005;152:16-18.
Bonilla C. Hidatidosis: Una zoonosis de múltiples Presentaciones clínicas. Revista Investigación y Desarrollo Social. Universidad Militar Nueva Granada. 2001;24:89-106.
Jenkins DJ, Romig T, Thompson RC. Emergence/re-emergence of Echinococcus spp. A global update. Int J Parasitol. 2005;35:1205-1219.
Romig T, Dinkel A, Mackenstedt U. The present situation of echinococcosis in Europe. Parasitol Int. 2006;55:S187-S191.
Moro P. Epidemiology and control of echinococcosis. UpToDate. Last updated October 15, 2014.
Salgado, DS, Suárez-Ognio, L & Cabrera, R. Características clínicas y epidemiológicas de la equinococosis quística registrados en un área endémica en los andes centrales del Perú. Neotrop Helminthol. 2007;1(2):69-83.
Moro P, Schantz P. Cystic echinococcosis in the Americas. Parasitol Int. 2006;55:S181-S186.
Perez V. Origen, desarrollo y extensión de la hidatidosis en América. Boletín de la oficina sanitaria panamericana. February 1949; 124-156.
Botero D. Parasitosis intestinales, cisticercosis e hidatidosis. Iatreia. 1990;3(3):165-171.
Alessandro A. Polycystic echinococcosis in tropical America: Echinococcus vogeli and E. oligarthrus. Acta Trop. 1997;67:43-65.
Torgerson, PR. Economic effects of echinococcosis. Acta Trop. 2003;85:113-118.
WHO Informal Working Group. International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Trop. 2003;85(2):253-261.
Gottstein B, Wang J, Blagosklonov O, et al. Echinococcus metacestode: In search of viability markers. Parasite. 2014;21:63. Epub; November 28, 2014.
Moro P. Clinical manifestations and diagnosis of echinococcosis. UpToDate. Last updated October 21, 2014.
Touma D, Sersté T, Ntounda R, et al. The liver involvement of the hydatid disease: A systematic review designed for the hepato-gastroenterologist. Acta Gastroenterol Belg. 2013;76(2): 210-218.
Stojkovic M, Junghanss T. Cystic and alveolar echinococcosis. Handb Clin Neurol. 2013;114:327-334.
Santivanez S, Garcia HH. Pulmonary cystic echinococcosis. Curr Opin Pulm Med. 2010;16:25.
Arinc S, Kosif A, Ertugrul M, et al. Evaluation of pulmonary hydatid cyst cases. Int J Surg. 2009;7:192.
Dziri C, Haouet K, Fingerhut A, Zaouche A. Management of cystic echinococcosis complications and dissemination: where is the evidence? World J Surg. 2009;33:1266.
Turgut AT, Altinok T, Topçu S, Koşar U. Local complications of hydatid disease involving thoracic cavity: Imaging findings. Eur J Radiol. 2009;70:49.
Díaz-Menéndez M, Pérez-Molina JA, Norman FF, et al. Management and outcome of cardiac and endovascular cystic echinococcosis. PLoS Negl Trop Dis. 2012;6:e1437.
Nourbakhsh A, Vannemreddy P, Minagar A, et al. Hydatid disease of the central nervous system: A review of literature with an emphasis on Latin American countries. Neurol Res. 2010;32:245.
Wuestenberg J, Gruener B, Oeztuerk S, at al. Diagnostics in cystic echinococcosis: Serology versus ultrasonography. Turk J Gastroenterol. 2014;25(4):398-404.
Soares Mdo C, Rodrigues AL, Moreira Silva CA, et al. Anatomo-clinical and molecular description of liver neotropical echinococcosis caused by Echinococcus oligarthrus in human host. Acta Trop. 2013;125(1):110-114.
Zimmerman DM, Douglass M, Reavill DR, Greiner EC. Echinococcus oligarthrus cystic hydatidosis in Brazilian agouti (Dasyprocta leporina). J Zoo Wildl Med. 2009;40(3):551-558.
Brunetti E, Kern P, Vuitton DA. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114(1):1-16.
Moro P. Treatment of echinococcosis. UpToDate. Last updated March 06, 2013.
Brunetti E, Filice C. Echinococcosis Hydatid Cyst Workup. Medscape. Last updated October 19, 2011.
Rinaldi F, Brunetti E, Neumayr A, et al. Cystic echinococcosis of the liver: A primer for hepatologists. World J Hepatol. 2014;6(5):293-305.
Stojkovic M, Rosenberger K, Kauczor HU, Junghanss T, Hosch W. Diagnosing and staging of cystic echinococcosis: How do CT and MRI perform in comparison to ultrasound? PLoS Negl Trop Dis. 2012;6(10):e1880.
McNanus D, Gray DJ, Zhang W, Yang Y. Diagnosis, treatment, and management of Echinococcosis. BMJ. 2012;344:e3866.
Bygott JM, Chiodini PL. Praziquantel: Neglected drug? Ineffective treatment? Or therapeutic choice in cystic hydatid disease? Acta Trop. 2009;111:95.
Tuxun T, Zhang JH, Zhao JM, et al. World review of laparoscopic treatment of liver cystic echinococcosis—914 patients. Int J Infect Dis. 2014;24:43-50.
Ormeci N. PAIR vs Örmeci technique for the treatment of hydatid cyst. Turk J Gastroenterol. 2014;25(4):358-364.
Neumayr A, Troia G, de Bernardis C, et al. Justified concern or exaggerated fear: the risk of anaphylaxis in percutaneous treatment of cystic echinococcosis-a systematic literature review. PLoS Negl Trop Dis. 2011;5:e1154.
Rinaldi F, De Silvestri A, Tamarozzi F, at al. Medical treatment versus "Watch and Wait" in the clinical management of CE3b echinococcal cysts of the liver. BMC Infect Dis. 2014;14:492.
Neumayr A, Tamarozzi F, Goblirsch S, Blum J, Brunetti E. Spinal cystic echinococcosis—a systematic analysis and review of the literature: Part 2. Treatment, follow-up and outcome. PLoS Negl Trop Dis. 2013;7(9):e2458.
Popa GL, Tanase I, Popa CA, et al. Medical and surgical management of a rare and complicated case of multivisceral hydatidosis: 18 years of evolution. New Microbiol. 2014;37(3):387-391. Epub Jul 1, 2014.
Pensel PE, Castro S, Allemandi D2, et al. Enhanced chemoprophylactic and clinical efficacy of albendazole formulated as solid dispersions in experimental cystic echinococcosis. Vet Parasitol. 2014;203(1-2):80-86.
Alvela-Suárez L, Velasco-Tirado V, Belhassen-Garcia M, et al. Safety of the combined use of praziquantel and albendazole in the treatment of human hydatid disease. Am J Trop Med Hyg. 2014;90(5):819-22.
Larrieu E, Zanini F. Critical analysis of cystic echinococcosis control programs and praziquantel use in South America, 1974-2010. Rev Panam Salud Publica. 2012;31(1):81-87.
Thompson RC. Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum. Clin Microbiol Infect. 2015:S1198-743X(15)00184-6. doi: 10.1016/j.cmi.2015.01.004. [Epub ahead of print]
Zheng H, Zhang W, Zhang L, et al. The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet. 2013;45(10):1168-1175. doi: 10.1038/ng.2757.
D'Alessandro A, Rausch RL, Morales GA, Collet S, Angel D. Echinococcus infections in Colombian animals. Am J Trop Med Hyg. 1981;30(6):1263-1276.
ICA. Sistema de información y vigilancia epidemiológica. Sanidad Animal 2008. Situación epidemiológica en Colombia con respecto de las enfermedades. 2008. Available at: http://www.ica.gov.co/getattachment/e205da92-1991-4de4-b412-29d6dae2ae40/2008-(1).aspx.
World Health Organization. Distribution of Echinococcus granulosus and cystic echinococcosis (hydatidosis), 2009. 2010. Available at: http://gamapserver.who.int/mapLibrary/Files/Maps/Global_echinococcosis_2009.png.
World Health Organization Office International des Epizooties. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. 2001; Paris, France: World Organization for Animal Health.
Eckert J, Deplazes P. Biological, epidemiological, and clinical aspects of echinococcosis: A zoonosis of increasing concern. Clin Microbiol Rev. 2004;17(1):107-135.
Martínez S, Restrepo CS, Carrillo JA, et al. Thoracic manifestations of tropical parasitic infections: A pictorial review. Radiographics. 2005;25(1):135-155.
Lichtember E. Equinococosis humana (quiste hidatídico) dos casos. Revista de la Facultad de Medicina (Bogotá). 1957; 25(3-4):119-127.
D'Alessandro A, Lega J, Vera MA. Cystic calcifications of the liver in Colombia. Echinococcosis or calcified abscesses? Am J Trop Med Hyg. 1966;15(6):908-913.
D'Alessandro A, Rausch RL, Morales GA, Collet S, Angel D. Echinococcus infections in Colombian animals. Am J Trop Med Hyg. 1981;30(6):1263-1276.
Rausch RL, D'Alessandro A, Rausch VR. Characteristics of the larval Echinococcus vogeli Rausch and Bernstein, 1972 in the natural intermediate host, the paca, Cuniculus paca L. (Rodentia: Dasyproctidae). Am J Trop Med Hyg. 1981;30(5):1043-1052.
Wells EA, D'Alessandro A, Morales GA, Angel D. Mammalian wildlife diseases as hazards to man and livestock in an area of the Llanos Orientales of Colombia. J Wildl Dis. 1981;17(1):153-162.
D'Alessandro A, Rausch RL, Cuello C, Aristizabal N. Echinococcus vogeli in man, with a review of polycystic hydatid disease in Colombia and neighboring countries. Am J Trop Med Hyg. 1979;28(2):303-317.
Cataño J. Cardiac echinococcosis, an unusual echocardiographic finding. Am J Trop Med Hyg. 2010;82(2):173.
Gómez G, Córdoba E, Córdoba A. Quiste hidatídico hepático. Rev Colomb Gastroenterol. 2003;18:183-186.
Morales GA, Guzman VH, Wells EA, Angel D. Polycystic echinococcosis in Colombia: The larval cestodes in infected rodents. J Wildl Dis. 1979;15(3):421-428.
Bolívar-Mejía A, Rodríguez-Morales AJ, Paniz-Mondolfi AE, Delgado O. Cardiovascular manifestations of human toxocariasis. Arch Cardiol Mex. 2013;83(2):120-129.
Hidron A, Vogenthaler N, Santos-Preciado JI, et al. Cardiac involvement with parasitic infections. Clin Microbiol Rev. 2010;23(2):324-349.
Franco-Paredes C, Rouphael N, Méndez J, et al. Cardiac manifestations of parasitic infections. Part 1: Overview and immunopathogenesis. Clin Cardiol. 2007;30(4):195-199.
Franco-Paredes C, Rouphael N, Méndez J, et al. Cardiac manifestations of parasitic infections. Part 2: Parasitic myocardial disease. Clin Cardiol. 2007;30(5):218-222.
Franco-Paredes C, Rouphael N, Méndez J, et al. Cardiac manifestations of parasitic infections. Part 3: Pericardial and miscellaneous cardiopulmonary manifestations. Clin Cardiol. 2007;30(6):277-280.
Pastore R, Vitali LH, Macedo Vde O, Prata A. A serological survey of the infection by Echinococcus sp. in the municipality of Sena Madureira, AC. Rev Soc Bras Med Trop. 2003;36(4):473-477.
Rodrigues-Silva R, Peixoto JR, de Oliveira RM, MagalhãesPinto R, Gomes DC. An autochthonous case of Echinococcus vogeli Rausch & Bernstein, 1972 polycystic echinococcosis in the state of Rondônia, Brazil. Mem Inst Oswaldo Cruz. 2002;97(1):123-126.
Thatcher VE. Neotropical echinococcosis in Columbia. Ann Trop Med Parasitol. 1972;66(1):99-105.
Howells RE, Schnur LF. Hydatid cysts in spiny rats in Amazonas, Colombia. Ann Trop Med Parasitol. 1978;72(4):395-396.
Bastidas A, Velásquez JC, Pérez CE. Derrame pleural eosinofílico por hidatidosis hepática: presentación de caso clínico y revisión de la literatura. Revista Med. 2008;16(1):45-55.
De la Hoz F, Alvis N, Narváez J, et al. Potential epidemiological and economical impact of two rotavirus vaccines in Colombia. Vaccine. 2010;28(22):3856-3864.
Mezones-Holguín E, Bolaños-Díaz R, Fiestas V, et al. Cost-effectiveness analysis of pneumococcal conjugate vaccines in preventing pneumonia in Peruvian children. J Infect Dev Ctries. 2014;8(12):1552-1562.
Branci S, Ewertsen C, Thybo S, et al. Cystic echinococcosis of the liver: Experience from a Danish tertiary reference center (2002-2010). J Travel Med. 2012;19(1):28-34.
Hellgren U, Botero-Kleiven S, Jansson A, Isaksson B. [Cystic echinococcosis. An imported severe parasitic disease.] Lakartidningen. 2012;109(1-2):30-33.
Ito A, Budke CM. Culinary delights and travel? A review of zoonotic cestodiases and metacestodiases. Travel Med Infect Dis. 2014;12(6 Pt A):582-591.
Rodriguez-Morales AJ, Schlagenhauf P. Zoonoses and travel medicine: "one world--one health". Travel Med Infect Dis. 2014;12(6 Pt A):555-556.
Cascio A, Bosilkovski M, Rodriguez-Morales AJ, Pappas G. The socio-ecology of zoonotic infections. Clin Microbiol Infect. 2011;17(3):336-342.
Pappas G, Cascio A, Rodriguez-Morales AJ. The immunology of zoonotic infections. Clin Dev Immunol. 2012;2012:208508.
Otero-Abad B1, Torgerson PR. A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis. 2013;7(6):e2249.
Mayor P, Baquedano LE, Sanchez E, et al. Polycystic echinococcosis in Pacas, Amazon region, Peru. Emerg Infect Dis. 2015;21(3):456-459.
Grozavu C, Ilias M, Pantile D. Multivisceral echinococcosis: Concept, diagnosis, management. Chirurgia (Bucur). 2014;109(6):758-768.
Wuestenberg J, Gruener B, Oeztuerk S, et al. Diagnostics in cystic echinococcosis: Serology versus ultrasonography. Turk J Gastroenterol. 2014;25(4):398-404.
Gomez I, Gavara C, López-Andújar R, et al. Review of the treatment of liver hydatid cysts. World J Gastroenterol. 2015;21(1):124-131.