A Canadian children's hospital's experience with cystic echinococcosis over 30 years: A case series
Publication: Journal of the Association of Medical Microbiology and Infectious Disease Canada
Volume 8, Number 4
Abstract
Abstract
Background:
Cystic echinococcosis (CE) or hydatid disease caused by the cestode Echinococcus granulosus sensu lato is an uncommon infection in Canada especially among children. There are limited reports describing the clinical presentation and management in Canadian children.
Methods:
The medical records of all children diagnosed with CE at a quaternary paediatric centre in Ontario between January 1988 and August 2021 were retrospectively reviewed. The clinical course, management, and outcomes of each case were summarized.
Results:
We report two paediatric cases of cystic echinococcosis (CE) in detail and review four additional cases seen at our institution over 33.5 years. The first case was a previously healthy 12-year-old boy with pulmonary CE resulting in unilateral lung collapse and mediastinal shift, who was presumedly infected while living in the Middle East. The second case was a previously healthy 3-year-old girl with pulmonary CE acquired locally in southern Ontario. Four other cases of CE with hepatic involvement (median age 12.5 years) were identified during the study period. Five out of six patients received both surgical and medical therapy.
Conclusion:
CE is a rare but serious disease seen in southern Canada that has historically been associated with travel or migration. Due to changes in urban wildlife landscapes and increased global migration, CE may become more prevalent in Canadian children. We describe the first locally acquired case in rural southern Ontario diagnosed at our centre. Prompt recognition of this infection in children by health care providers is important to prevent morbidity and mortality.
Résumé
Historique :
L’échinococcose kystique (ÉK), ou hydatidose, causée par le cestode Echinococcus granulosus sensu lato, est une infection peu courante au Canada, particulièrement chez les enfants. Peu de rapports en décrivent la présentation clinique et la prise en charge chez les enfants canadiens.
Méthodologie :
Les auteurs ont procédé à l’analyse rétrospective des dossiers médicaux de tous les enfants ayant reçu un diagnostic d’ÉK dans un centre pédiatrique de soins quaternaires ontarien entre janvier 1988 et août 2021. Ils ont résumé l’évolution clinique, la prise en charge et le résultat clinique de chaque cas.
Résultats :
Les auteurs font un compte rendu détaillé de deux cas pédiatriques d’ÉK et analysent quatre autres cas observés à leur établissement sur une période de 33,5 ans. Le premier cas d’ÉK pulmonaire a touché un garçon de 12 ans auparavant en santé, probablement infecté alors qu’il habitait au Moyen-Orient, et a entraîné un collapsus pulmonaire unilatéral et une déviation médiastinale. Le deuxième cas d’ÉK pulmonaire a été observé chez une fillette de trois ans auparavant en santé qui a été infectée dans le sud de l’Ontario. Les auteurs ont relevé quatre autres cas d’ÉK comportant une atteinte hépatique (âge médian de 12,5 ans) pendant la période de l’étude. Cinq des six patients ont reçu à la fois un traitement chirurgical et médical.
Conclusion :
L’ÉK est une maladie rare, mais grave dans le sud du Canada. Elle était auparavant associée à un voyage ou une migration. En raison des changements aux paysages fauniques urbains et de la migration mondiale accrue, elle pourrait devenir plus prévalente chez les enfants canadiens. Les auteurs décrivent les premiers cas d’acquisition dans les régions rurales du sud de l’Ontario, diagnostiqués à leur centre. Il est important que les dispensateurs de soins dépistent cette infection rapidement chez les enfants pour éviter la morbidité et la mortalité.
Introduction
Cystic echinococcosis or hydatid disease, is a neglected zoonosis caused by the larval stage of the cestode Echinococcus granulosus sensu lato (s.l.)(1–3). CE occurs worldwide with the highest incidence in the Mediterranean, eastern Europe, northern Africa, Central Asia, and South America. Molecular studies have identified several distinct strains within the E. granulosis sensu lato (s.l.) complex that differ in their geographic distributions and host range (4,5). The pastoral life cycle of E. granulosus sensu stricto (s.s.) typically involves dogs as definitive hosts and ruminant animals (eg, sheep, goats) as intermediate hosts (2,3). In Canada, E. canadensis is the endemic species and wild canines (eg, wolves, foxes, coyotes) or domestic dogs, and moose, elk, reindeer or caribou may serve as definitive and intermediate hosts in the sylvatic life cycle, respectively (6). Humans are accidental hosts, infected through ingestion of parasite eggs in food or water contaminated by dog feces (2,3,6,7). CE is an uncommon infection in Canada (3,6,8) and rare in children (9). However, with changes in the urban wildlife landscape—owing to human encroachment on natural habitats—and increasing global migration, CE may become more prevalent among children in Canada (6,10,11). We report two cases in detail, a case of severe case of pulmonary CE in a child who had come to Canada as a refugee from the Middle East and the first locally acquired case of pulmonary CE diagnosed at our centre as illustrative cases highlighting the epidemiology, presentation, diagnosis, and management of this condition. We also identify four other cases seen over a 33.5-year period at the Hospital for Sick Children, a paediatric quaternary care centre in Toronto, Ontario, Canada.
Methods
We performed a retrospective chart review of all paediatric patients (age <18 years) with a diagnosis of CE from January 1, 1988 to August 1, 2021 at the Hospital for Sick Children in Toronto, Ontario, Canada. Possible cases of CE were identified using International Classification of Disease (ICD) Ninth Edition codes [ICD-9 122.0 to 122.9] from January 1, 1988 to March 31, 2002, and ICD-10 codes B67.8, B67.9, and B71.9 from April 1, 2002 to August 1, 2021. Patients were included if they had: (1) compatible histopathologic findings, (2) positive serology with compatible clinical presentation, or (3) a clinical presentation, epidemiology, and imaging compatible with CE and were managed as such, but with no histopathologic or serologic evidence of CE. Medical records of children with CE were reviewed for the following parameters: demographics, symptoms, cyst features, serology, management, and outcomes. Ethics approval was obtained from our institutional research ethics board (REB# 1000043659) and consent for the highlighted case reports were obtained from the families.
Results
A total of 46 hospital records were identified using ICD-9 and -10 codes during the study period. Forty cases were excluded after medical charts were reviewed and were determined to have a diagnosis other than CE based on absence of epidemiologic risk factors, imaging findings, histopathology, and other microbiologic tests. Six children with CE were included in the study, with demographics of each outlined in Table 1. The median age of the patients was 12.5 years (range 3–17 years) and there were four males and two females. All patients except for patient 2 were foreign born. The clinical presentation, diagnostic features, and management of each patient are outlined in Table 2.
| Patient | Age (y) | Sex | Past medical history | Country of origin | Travel | Animal exposure |
|---|---|---|---|---|---|---|
| 1* | 12 | M | Healthy | Syria | None since immigration | No known exposure |
| 2* | 3 | F | Healthy | Canada | None | Household dog, farm animals |
| 3 | 10 | M | Healthy | India | None since immigration | Farm animals |
| 4 | 17 | F | History of hydatid disease | Romania | None since immigration | No known exposure |
| 5 | 13 | M | Healthy | Romania | None since immigration | No known exposure |
| 6 | 15 | M | Healthy | Afghanistan | None since immigration | Farm animals |
*
Highlighted in the introduction
| Patient | Symptoms | Cyst location | No. of cysts | Diameter of cyst(s) (cm) | Serology | Medical therapy | Surgical therapy |
|---|---|---|---|---|---|---|---|
| 1 | Fever, weight loss, night sweats | Lung | 1 (40+ daughter cysts) | 20 | EIA reactive | ABZ + PZQ | Thoracotomy, cystectomy, lobectomy |
| 2 | Fever, cough | Lung | 3 | 3.5 | EIA non-reactive* | ABZ + PZQ | Thoracotomy, Cystectomy |
| 3 | Incidental finding after trauma | Liver | 1 | 10 | IHA reactive (1:2048) | ABZ | PAIR |
| 4 | Abdominal pain, fever, diarrhea, and vomiting | Liver | 1 | 10 | IHA non-reactive | ABZ | Unknown† |
| 5 | Abdominal pain and vomiting | Liver | 1 | 5 | N/A (Confirmed on pathology) | ABZ + PZQ | Cystectomy (rupture) |
| 6 | Anaphylaxis, abdominal pain, fever, vomiting | Liver | 1 | 7 | IHA reactive (1:1048576) | ABZ + PZQ | Cystectomy (failed medical therapy) |
*
Tested for both E. granulosus and E. multilocularis EIA
†
Follow-up in adult hospital
EIA = enzyme immunoassay, IHA = indirect hemagglutination; PAIR = puncture, aspiration, injection of protoscolecide, re-aspiration; ABZ = albendazole; PZQ = praziquantel
All six patients had CE based on histopathology, serology, and/or imaging. Four patients had hepatic disease and two had pulmonary disease. All patients except for patient 3 were symptomatic at the time of presentation. Patient 4 had been previously diagnosed with liver CE and was treated in Romania with radical surgery followed by a course of albendazole. While in Canada, this patient was non-adherent to albendazole therapy and re-presented to our institution. Given the patient's age, the patient was referred to an adult hospital for further management and no further clinical details are available for this study. All patients followed at our institution (five patients) required a surgical intervention (Table 2). Four patients were treated with a combination of albendazole and praziquantel and two with albendazole monotherapy. Medical therapy duration ranged from 1 to 6 months.
Case 1
A healthy 12-year-old boy was referred to a tertiary care children's hospital after a chest radiograph (CXR) obtained in the community to investigate fever, drenching night sweats, and an 8-kg weight loss over 2 months revealed an unexpected finding of total and diffuse left hemi-thorax opacification. The child was seen in the emergency department where despite this impressive finding, he had no dyspnea, orthopnea, or hypoxia. At this hospital, a CT scan of the chest was completed revealing a large, 12 × 13 × 20 cm complex multi-cystic mass with associated near-complete left lung collapse, mediastinal shift, and prominent superior diaphragmatic lymph nodes (Figure 1). Neck and abdominal CT completed at the same time as the CT chest to investigate for possible malignancy, were unremarkable. Given the concern for potential impact of the mass on cardiac output, an echocardiogram was completed, which was also unremarkable. MRI of the chest was subsequently performed showing again the multi-cystic left thoracic mass (Figure 1).
Figure 1: Case 1. Left pulmonary cystic echinococcosis in a 12-year-old male.
(A) Coronal reformatted and (B) axial contrast-enhanced CT images show a large left-sided cystic mass with daughter cysts in its inferomedial aspect (white arrows) causing significant mediastinal shift. (C) Coronal contrast-enhanced fat-suppressed T1-weighted MR image shows a large mass (black arrows) occupying most of the left hemithorax and causing shift of the heart and mediastinum towards the right. The mass has a multicystic appearance with a large mother cyst (*) and smaller daughter cysts inferomedially (white arrow). (D) Axial fat-suppressed T2-weighted MR image through the lower chest acquired in right lateral decubitus position shows that the mother cyst (*) is predominantly hyperintense with intermediate and low signal intensity debris seen in the dependent aspect medially (black arrows) representing fragmented membranes. Daughter cysts of higher signal intensity are seen medially (white arrows)
A complete blood count revealed slight thrombocytosis (394 × 109/L, reference range: 130–380 × 109/L) but otherwise white blood cell count including eosinophil count was within normal limits. He had elevated C-reactive protein (94.4 mg/L, reference range: <10 mg/L) and erythrocyte sedimentation rate (70 mm/h, reference range: <30 mm/h). Serologic testing for E. granulosus IgG by enzyme immunoassay (EIA) was reactive with an index of 9.01 (reactive threshold >1.1).
In discussion with international clinicians with extensive experience in the management of complex cases of echinococcal disease, the decision was made to transfer him to the Hospital for Sick Children for surgical intervention. Empiric albendazole (15 mg/kg/d divided twice daily, maximum: 400 mg/dose) and praziquantel (25 mg/kg/d given once daily) were commenced 3 days prior to his procedure. The procedure consisted of a left anterolateral thoracotomy with catheter insertion through pleura into the mother cyst cavity, aspiration of cystic fluid, infusion of 3% normal saline into the cyst cavity, and re-aspiration of 1980 mL of fluid with minimal spillage. A subsequent total cystectomy of the mother cyst and lobectomy of the left lower lobe to remove two highly adherent smaller daughter cysts were performed. Microscopic examination of cyst membranes showed degenerating parasitic structures, while the cystic fluid showed hooklets consistent with CE.
The child was born in Syria and moved to Lebanon at 2 years of age before coming to Canada as a refugee when he was 8 years old, where he has remained ever since. The family lives in an urban centre in southern Quebec and have had no pets or other significant exposure to animals in Canada or elsewhere. The family was screened by their family doctor with CXR and abdominal ultrasound and were all subsequently negative.
The patient recovered well from his operation and was discharged home on postoperative day 15. He completed treatment for CE with 3 months of albendazole (15 mg/kg/d divided twice daily, maximum: 400 mg/dose) and praziquantel (25 mg/kg/d given once daily), followed by 3 months of albendazole monotherapy (15 mg/kg/d divided twice daily, maximum: 400 mg/dose), for a total treatment duration of 6 months. The patient remained well, regained the weight he lost, and returned to normal activities including sports. A follow-up CXR at the end of therapy was normal with good lung expansion, and a CT scan of the chest approximately 3 months after completion of medical treatment, 9 months after his surgical procedure, showed no evidence of disease recurrence in the lung parenchyma.
Case 2
A healthy Canadian-born 3-year-old girl was referred to the Hospital for Sick Children following an incidental finding of three round opacities in the left lung identified on CXR, during an admission for an uncomplicated ipsilateral pneumonia. Her pneumonia fully resolved after an appropriate course of antibiotics, however the cystic lesions remained unchanged on follow-up CXR several months later. She was otherwise asymptomatic and had no respiratory symptoms prior to admission.
Chest ultrasound and CT demonstrated three homogeneous, avascular, anechoic, fluid-filled cysts with smooth, well circumscribed walls, measuring up to 3.5 cm, in the left lower lung lobe (Figure 2). Due to suspicion of CE, further imaging with abdominal ultrasound, echocardiogram, and whole-body MRI excluded extrapulmonary involvement. Blood work including eosinophil count was unremarkable and serologic testing for E. granulosus IgG by enzyme immunoassay (EIA) was non-reactive.
Figure 2: Case 2. Left pulmonary cystic echinococcosis in a 3-year-old girl.
(A) AP chest radiograph shows three round nodules in the left lung (black arrows). (B) Axial contrast-enhanced CT image shows a round hypodense nodule in the left lower lobe (white arrows). The attenuation characteristics suggest a cystic lesion. No calcifications or surrounding halo were seen
After extensive discussion with infectious diseases, surgery, and paediatrics, empiric albendazole (15 mg/kg/d divided twice daily, maximum: 400 mg/dose) and praziquantel (25 mg/kg/d divided twice daily) were commenced 3 days prior to excisional total cystectomy, which was successfully conducted without fluid leakage. Microscopic examination showed that the cyst wall was comprised of inner germinal and outer laminated hyaline layers, and contained multiple protoscolices with hooklets and calcareous corpuscles, which were consistent with CE (Figure 3).
Figure 3: Case 2. Light microscopy of lung cystic fluid aspirated from Case 2 using hematoxylin and eosin stain.
(A) The cyst wall comprising inner germinal layer and outer acellular laminated hyaline layer (×100); (B) part of the brood capsule with protoscolices, calcareous corpuscules, and germinal layer (×200); (C, D) protoscolices with row of refractile hooklets at high magnification (×400)
The child has never traveled outside of Ontario, and lives with her family on a farm in a rural area of southern Ontario with several dogs, a sheep, and other farm animals. The family denied any history of hunting with dogs. Subsequent screening of other family members using CXR and abdominal ultrasound was negative. Due to the child’s diagnosis, household pets were also screened by stool examination, revealing echinococcosis affecting one dog. The patient completed treatment for CE with 6 weeks of albendazole (15 mg/kg/d divided twice daily, maximum: 400 mg/dose) and praziquantel (25 mg/kg/d divided twice daily), followed by albendazole monotherapy (15 mg/kg/d divided twice daily, maximum: 400 mg/dose) for a total of 4 months. The patient remained well and a follow-up CXR at the end of therapy was normal. A follow-up chest MRI approximately 18 months following completion of medical treatment showed no evidence of cysts in the lung parenchyma.
Discussion
CE is a rare but important infection to recognize as it can lead to significant morbidity and in some circumstances, death. CE causes tissue cysts, primarily in the liver followed by lung (1,2,6). Many patients are initially infected in childhood but do not manifest symptoms until adulthood at which point a sufficient interval has elapsed to enable mass effect or compressive symptoms due to size (eg, biliary or bronchial obstruction, abdominal distension, headache). The latent period can last years to decades and mean cyst growth can be as slow as 0.7 cm over 10 years, therefore many are diagnosed incidentally (12), particularly in children. Symptoms occur secondary to cystic complications such as rupture, compression of surrounding structures, hemorrhage, secondary bacterial infection, or organ failure. An anaphylactic and potentially fatal reaction following cyst leakage from minor trauma can occur (9,13).
Over a 33.5-year period at the Hospital for Sick Children, in Toronto, Ontario, Canada, six cases of CE were identified. Five out of six patients were above the age of 10 years. This is likely attributed to the long latency from primary infection to the onset of clinical symptoms (12). While uncommon, CE can present in early childhood. In a retrospective review of CE in children in Turkey, only 5/152 patients were under the age of 5 (14). One distinguishing feature of CE in children is the ratio of lung to liver involvement. Compared to adults, lung involvement is more common in children (14–16). Two patients in our case series had pulmonary involvement and only one was under the age of 5.
Diagnosis of CE in children is based on a combination of clinical presentation, appropriate epidemiological exposure, medical imaging suggestive of disease, serological markers, microscopy, and histopathology (1). In our case series, three out of the five patients with completed serologic assays had reactive tests. Sensitivity and specificity can vary depending on the type of assay used and clinical factors such as stage of cyst and cyst location (17,18). Until 2016, the Provincial Health Ontario Laboratory (PHOL) utilized complement fixation test (CFT) as initial screening, followed by confirmatory indirect hemagglutination (IHA). Both tests have poor sensitivity and specificity (17,18). In 2016, the PHOL replaced CFT and IHA with an immunoglobulin G (IgG) EIA. IgG EIA has an estimated sensitivity of 80%–90% for liver involvement, however, sensitivity decreases for lung (60%–85%) or other organ involvement (17–19). Unsurprisingly, patient 2 with pulmonary CE had negative IgG EIA. Patient age influences the reliability of serology, and often children with echinococcosis aged 3–15 years may have a nominal antibody response (20). The reason for the difference in sensitivity between cyst sites is not well understood, but in part has been attributed to the higher immunological response to hepatic cysts compared to cysts at other anatomic sites (21–23). Cyst wall compromise through rupture or fissuring causes a robust antibody response, regardless of anatomic location, while calcified or senescent cysts less reliably generate an immunologic response (24).
Treatment of paediatric CE depends on the size and location of the cysts, and if any complications are present (1,2). Management options that may be considered depending on location and staging of the cyst include observation, antihelminthic drugs (albendazole with or without praziquantel), surgery, and/or percutaneous procedures such as puncture, aspiration, injection of protoscolecide, and re-aspiration (PAIR) (1,25,26). Albendazole is the primary chemotherapeutic agent for CE, however some observational data suggest that combined therapy with albendazole and praziquantel is superior to albendazole alone due to higher scolicidal and anti-cyst activity (27,28). For cysts located in the liver, treatment is guided by the World Health Organization diagnostic classification. Stage CE1 and CE3a cysts less than 5 cm in diameter can be managed with albendazole alone, whereas cysts larger than 5 cm require albendazole and PAIR. Stage CE2 and CE3b cysts require medical management in combination with a non-PAIR technique or surgery. Stage CE4 and CE5 cysts are inactive and can be managed by observation only (1).
Five out of six patients in our case series were foreign born. However, with increasing changes in climate and animal migration, the geographic distribution of E. granulosus sensu lato complex of species is likely to expand. Locally acquired human cases of E. canadensis have been well documented in Arctic and sub-Arctic regions of Canada (3,6–8,29). However, patient 2 had CE despite having never left southern Ontario and is the first locally acquired case diagnosed at our institution in over three decades.
The retrospective collection of data from a single quaternary paediatric centre and the small number of cases identified are key limitations of this study. CE is an infection that is challenging to diagnose and requires a high index of suspicion, particularly in children and centres from non-endemic regions. The lack of a reliable gold standard diagnostic assay further compounds this diagnostic challenge and may result in incorrect ICD-coding and underdiagnosis. ICD-9 and 10 codes were key in case ascertainment for this study and as a result the true number of cases encountered at our centre may be underestimated by the study findings. This series also captures only those cases who were symptomatic enough from CE to seek medical care or were unwell due to another illness that prompted diagnostic imaging. For some patients, the management happened in other countries or institutions and those records were unavailable to us.
In conclusion, CE is an uncommon infection in Canadian children. Diagnosis can be challenging and relies on eliciting epidemiological exposures, appropriate imaging, and complimentary serologic testing. As the geographic distribution of E. canadensis moves further south in Canada, prompt recognition of this infection is important to prevent morbidity and mortality.
Registry and the Registration No. of the Study/Trial:
N/A
Funding:
No funding was received for this work.
Peer Review:
This manuscript has been peer reviewed.
Animal Studies:
N/A
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Journal of the Association of Medical Microbiology and Infectious Disease Canada
Volume 8 • Number 4 • December 2023
Pages: 262 - 271
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© Association of Medical Microbiology and Infectious Disease Canada (AMMI Canada), 2023. This article is free to read to all interested readers, immediately upon publication. For their own personal use, users may read, download, print, search, or link to the full text. Manuscripts published in the Journal of the Association of Medical Microbiology and Infectious Disease Canada are copyrighted to the Association of Medical Microbiology and Infectious Disease Canada (AMMI Canada). Requests for permission to reproduce this article should be made to the University of Toronto Press using the Permission Request Form: https://jammi.utpjournals.press/journal-policies#_copyright or by email: [email protected].
History
Received: 30 November 2022
Revision received: 3 August 2023
Accepted: 19 August 2023
Published online: 16 January 2024
Published in print: December 2023
Keywords:
Mots-Clés :
Authors
Contributors:
Conceptualization, F Razik, KL Schwartz, SK Morris; Methodology, F Razik, KL Schwartz, SK Morris; Formal Analysis, K Kazmi, C Krueger, W Wong; Investigation, K Kazmi, C Krueger, W Wong; Data Curation, K Kazmi, F Razik; Writing – Original Draft, K Kazmi, C Krueger, W Wong; Writing – Review & Editing, K Kazmi, C Krueger, W Wong, R Baertschiger, C Hui, A Nagy, OM Navarro, F Razik, KL Schwartz, AK Boggild, SK Morris; Visualization, K Kazmi, C Krueger, A Nagy, OM Navarro; Supervision, SK Morris; Project Administration, K Kazmi, SK Morris.
Disclosures:
The authors have nothing to disclose.
Ethics Approval:
This study was approved by the Hospital for Sick Children Research Ethics Board, Toronto, Ontario, Canada on January 15, 2014.
Informed Consent:
The authors confirm that informed patient consent has been secured from all patients whose personal information is included in the manuscript or the parents or guardians of minors.
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Journal of the Association of Medical Microbiology and Infectious Disease Canada 2024 8:4, 262-271
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