Imaging of toxocariasis

Christoph F. Dietrich; Carmen-Michaela Cretu; Nathan S. S. Atkinson; W. J. Lee; Joachim Richter; Xin-Wu Cui; Zeno Sparchez; Yi Dong

doi:10.1055/a-0821-7220

Zeitschrift für Gastroenterologie, Table of Contents

Z Gastroenterol 2019; 57(03): 327-334
DOI: 10.1055/a-0821-7220

Übersicht

Imaging of toxocariasis

Bildgebung der Toxocarias

Christoph F. Dietrich

¹Department of Internal Medicine 2, Caritas Krankenhaus, Bad Mergentheim, Germany

,

Carmen-Michaela Cretu

²Department of Parasitology, Carol Davila University of Medicine and Pharmacy, Colentina Clinical Hospital, Bucharest, Romania

,

Nathan S. S. Atkinson

³Department of Gastroenterology, Waitemata District Health Board, Auckland, NZ

,

W. J. Lee

⁴Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

,

Joachim Richter

⁵Institute of Tropical Medicine and International Health Charité Universitätsmedizin, Berlin, Germany

,

Xin-Wu Cui

⁶Xin-Wu Cui, Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China

,

Zeno Sparchez

⁷3rd Medical Department, University of Medicine and Pharmacy “Iuliu Hatieganu”, Institute for Gastroenterology and Hepatology “O. Fodor” Cluj-Napoca, Romania

,

Yi Dong

⁸Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai, China

› Author Affiliations

Abstract

Zusammenfassung

Parasitäre Erkrankungen werden in Europa relativ selten diagnostiziert und behandelt. Somit sind auch klinische Besonderheiten und bildgebende Merkmale weniger bekannt. In den heutigen Zeiten von Migration und weltweiter Flüchtlingsströme ist die Kenntnis parasitärer Infektionen zunehmend von Bedeutung. Anhand von klinischen Beschreibungen der Echinokokkose, Schistosomiasis, Fasciolosis und Ascariasis wurden entsprechende Berichte in der Zeitschrift für Gastroenterologie publiziert. In der hier präsentierten Veröffentlichung werden klinische Besonderheiten und Bildgebungsmerkmale der Toxocariasis diskutiert.

Abstract

Parasitic diseases are rarely encountered in Europe and the clinical and imaging features are generally not well known. In the era of worldwide migration and refugees, knowledge of such diseases has gained importance as illustrated by multiple recently published reports of hydatid diseases, schistosomiasis, fasciolosis, and ascariasis. Herewith we describe the clinical and imaging features along with current treatment strategies of toxocariasis.

Schlüsselwörter

Parasiten - Leitlinien - Ultraschall - Leber - Granulome

Key words

parasite - guideline - ultrasound - liver - granuloma

Full Text

References

References
1 Dietrich CF, Lorentzen T, Appelbaum L. et al. EFSUMB guidelines on interventional ultrasound (INVUS), part III – abdominal treatment procedures (long version). Ultraschall in Med 2016; 37: E1-E32
2 Dietrich CF, Lorentzen T, Appelbaum L. et al. EFSUMB guidelines on interventional ultrasound (INVUS), part III – abdominal treatment procedures (short version). Ultraschall in Med 2016; 37: 27-45
3 Dietrich CF, Hocke M. Interventionelle Therapie der Echinokokkose. In: Dietrich CF, Nurnberg D. eds. Interventionelle Sonographie. Stuttgart: Thieme Verlag; 2011: 240-256
4 Dietrich CF, Mueller G, Beyer-Enke S. Cysts in the cyst pattern. Z Gastroenterol 2009; 47: 1203-1207
5 Brunetti E, Tamarozzi F, Macpherson C. et al. Ultrasound and cystic echinococcosis. Ultrasound Int Open 2018; 4: E70-E78
6 Dietrich CF, Sharma M, Chaubal N. et al. Ascariasis imaging: pictorial essay. Z Gastroenterol 2017; 55: 479-489
7 Richter J, Azoulay D, Dong Y. et al. Ultrasonography of gallbladder abnormalities due to schistosomiasis. Parasitol Res 2016; 115: 2917-2924
8 Richter J, Botelho MC, Holtfreter MC. et al. Ultrasound assessment of schistosomiasis. Z Gastroenterol 2016; 54: 653-660
9 Dietrich CF, Kabaalioglu A, Brunetti E. et al. Fasciolosis. Z Gastroenterol 2015; 53: 285-290
10 Dietrich CF, Lembcke B, Jenssen C. et al. Intestinal ultrasound in rare gastrointestinal diseases, update, part 1. Ultraschall in Med 2014; 35: 400-421
11 Azam D, Ukpai OM, Said A. et al. Temperature and the development and survival of infective Toxocara canis larvae. Parasitol Res 2012; 110: 649-656
12 Centers for Disease Control and Prevention. Ocular toxocariasis--United States, 2009–2010. Morb Mortal Wkly Rep 2011; 60: 734-736
13 Liu EW, Chastain HM, Shin SH. et al. Seroprevalence of antibodies to Toxocara species in the United States and associated risk factors, 2011–2014. Clin Infect Dis 2018; 66: 206-212
14 Hotez PJ, Wilkins PP. Toxocariasis: America’s most common neglected infection of poverty and a helminthiasis of global importance?. PLoS Negl Trop Dis 2009; 3: e400
15 Mok CH. Visceral larva migrans. A discussion based on review of the literature. Clin Pediatr (Phila) 1968; 7: 565-573
16 Won KY, Kruszon-Moran D, Schantz PM. et al. National seroprevalence and risk factors for Zoonotic Toxocara spp. infection. Am J Trop Med Hyg 2008; 79: 552-557
17 Mohamed AS, Moore GE, Glickman LT. Prevalence of intestinal nematode parasitism among pet dogs in the United States (2003–2006). J Am Vet Med Assoc 2009; 234: 631-637
18 Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 2003; 16: 265-272
19 Glickman LT, Cypess RH. Toxocara infection in animal hospital employees. Am J Public Health 1977; 67: 1193-1195
20 Rubinsky-Elefant G, Hirata CE, Yamamoto JH. et al. Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol 2010; 104: 3-23
21 Lim JH. Toxocariasis of the liver: visceral larva migrans. Abdom Imaging 2008; 33: 151-156
22 Baaten GG, Sonder GJ, van Gool T. et al. Travel-related schistosomiasis, strongyloidiasis, filariasis, and toxocariasis: the risk of infection and the diagnostic relevance of blood eosinophilia. BMC Infect Dis 2011; 11: 84
23 Van Den Broucke S, Kanobana K, Polman K. et al. Toxocariasis diagnosed in international travelers at the Institute of Tropical Medicine, Antwerp, Belgium, from 2000 to 2013. PLoS Negl Trop Dis 2015; 9: e0003559
24 Smith H, Holland C, Taylor M. et al. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol 2009; 25: 182-188
25 McGuinness SL, Leder K. Global burden of toxocariasis: a common neglected infection of poverty. Curr Trop Med Rep 2014; 1: 52
26 Taylor MR, Keane CT, O’Connor P. et al. Clinical features of covert toxocariasis. Scand J Infect Dis 1987; 19: 693-696
27 Glickman LT, Magnaval JF, Domanski LM. et al. Visceral larva migrans in French adults: a new disease syndrome?. Am J Epidemiol 1987; 125: 1019-1034
28 Good B, Holland CV, Taylor MR. et al. Ocular toxocariasis in schoolchildren. Clin Infect Dis 2004; 39: 173-178
29 Paul M, Stefaniak J, Twardosz-Pawlik H. et al. The co-occurrence of Toxocara ocular and visceral larva migrans syndrome: a case series. Cases J 2009; 2: 6881
30 Stewart JM, Cubillan LD, Cunningham Jr ET. Prevalence, clinical features, and causes of vision loss among patients with ocular toxocariasis. Retina 2005; 25: 1005-1013
31 Suh LH, Sweeney DA, Jun AS. A 33-year-old man with a white pupil. Clin Infect Dis 2006; 43: 1043-1044
32 Kuenzli E, Neumayr A, Chaney M. et al. Toxocariasis-associated cardiac diseases--a systematic review of the literature. Acta Trop 2016; 154: 107-120
33 Jabbour RA, Kanj SS, Sawaya RA. et al. Toxocara canis myelitis: clinical features, magnetic resonance imaging (MRI) findings, and treatment outcome in 17 patients. Medicine (Baltimore) 2011; 90: 337-343
34 Huntley CC, Costas MC, Lyerly A. Visceral larva migrans syndrome: clinical characteristics and immunologic studies in 51 patients. Pediatrics 1965; 36: 523-536
35 Snyder C. Visceral larva migrans – ten years’ experience. Pediatrics 1965; 36: 523
36 Gavignet B, Piarroux R, Aubin F. et al. Cutaneous manifestations of human toxocariasis. J Am Acad Dermatol 2008; 59: 1031-1042
37 Fan CK, Holland CV, Loxton K. et al. Cerebral toxocariasis: silent progression to neurodegenerative disorders?. Clin Microbiol Rev 2015; 28: 663-686
38 Cooper PJ. Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol 2009; 9: 29-37
39 Li L, Gao W, Yang X. et al. Asthma and toxocariasis. Ann Allergy Asthma Immunol 2014; 113: 187-192
40 Glickman L, Schantz P, Dombroske R. et al. Evaluation of serodiagnostic tests for visceral larva migrans. Am J Trop Med Hyg 1978; 27: 492-498
41 Jones JL, Kruszon-Moran D, Won K. et al. Toxoplasma gondii and Toxocara spp. co-infection. Am J Trop Med Hyg 2008; 78: 35-39
42 Rodriguez-Caballero A, Martinez-Gordillo MN, Medina-Flores Y. et al. Successful capture of Toxocara canis larva antigens from human serum samples. Parasit Vectors 2015; 8: 264
43 Magnaval JF, Fabre R, Maurieres P. et al. Application of the western blotting procedure for the immunodiagnosis of human toxocariasis. Parasitol Res 1991; 77: 697-702
44 Roig J, Romeu J, Riera C. et al. Acute eosinophilic pneumonia due to toxocariasis with bronchoalveolar lavage findings. Chest 1992; 102: 294-296
45 Fillaux J, Magnaval JF. Laboratory diagnosis of human toxocariasis. Vet Parasitol 2013; 193: 327-336
46 Fogt-Wyrwas R, Jarosz W, Mizgajska-Wiktor H. Utilizing a polymerase chain reaction method for the detection of Toxocara canis and T. cati eggs in soil. J Helminthol 2007; 81: 75-78
47 Pawlowski Z. Toxocariasis in humans: clinical expression and treatment dilemma. J Helminthol 2001; 75: 299-305
48 de Visser L, Rothova A, de Boer JH. et al. Diagnosis of ocular toxocariasis by establishing intraocular antibody production. Am J Ophthalmol 2008; 145: 369-374
49 Eberhardt O, Bialek R, Nagele T. et al. Eosinophilic meningomyelitis in toxocariasis: case report and review of the literature. Clin Neurol Neurosurg 2005; 107: 432-438
50 Nicoletti A. Toxocariasis. Handb Clin Neurol 2013; 114: 217-228
51 Field V, Gautret P, Schlagenhauf P. et al. Travel and migration associated infectious diseases morbidity in Europe, 2008. BMC Infect Dis 2010; 10: 330
52 Kayes SG. Human toxocariasis and the visceral larva migrans syndrome: correlative immunopathology. Chem Immunol 1997; 66: 99-124
53 Dietrich CF, Rudd L. The EFSUMB website, a guide for better understanding. Med Ultrason 2013; 15: 215-223
54 Dietrich CF, Rudd L, Saftiou A. et al. The EFSUMB website, a great source for ultrasound information and education. Med Ultrason 2017; 19: 102-110
55 Ishibashi H, Shimamura R, Hirata Y. et al. Hepatic granuloma in toxocaral infection: role of ultrasonography in hypereosinophilia. J Clin Ultrasound 1992; 20: 204-210
56 Jain R, Sawhney S, Bhargava DK. et al. Hepatic granulomas due to visceral larva migrans in adults: appearance on US and MRI. Abdom Imaging 1994; 19: 253-256
57 Zachariah SB, Zachariah B, Varghese R. Neuroimaging studies of cerebral “visceral larva migrans” syndrome. J Neuroimaging 1994; 4: 39-40
58 Baldisserotto M, Conchin CF, Soares MG. et al. Ultrasound findings in children with toxocariasis: report on 18 cases. Pediatr Radiol 1999; 29: 316-319
59 Sakai S, Shida Y, Takahashi N. et al. Pulmonary lesions associated with visceral larva migrans due to Ascaris suum or Toxocara canis: imaging of six cases. Am J Roentgenol 2006; 186: 1697-1702
60 Jang EY, Choi MS, Gwak GY. et al. Enhanced resolution of eosinophilic liver abscess associated with toxocariasis by albendazole treatment. Korean J Gastroenterol 2015; 65: 222-228
61 Coskun F, Akinci E. Hepatic toxocariasis: a rare cause of right upper abdominal pain in the emergency department. Turkiye Parazitol Derg 2013; 37: 151-153
62 Sarda AK, Kannan R. Visceral larva migrans masquerading as liver secondaries. J Indian Med Assoc 1992; 90: 302
63 Chang S, Lim JH, Choi D. et al. Hepatic visceral larva migrans of Toxocara canis: CT and sonographic findings. Am J Roentgenol 2006; 187: W622-W629
64 Azuma K, Yashiro N, Kinoshita T. et al. Hepatic involvement of visceral larva migrans due to Toxocara canis: a case report--CT and MR findings. Radiat Med 2002; 20: 89-92
65 Kaur J, Gupta A, Wadhwa N. Hepatic visceral larva migrans causing hepatic venous thrombosis and prolonged fever. Indian Pediatr 2017; 54: 882-884
66 Ghoroobi J, Mohajerzadeh L, Khoddami M. et al. Abdominal mass secondary to human toxocariasis. APSP J Case Rep 2017; 8: 4
67 Mazur-Melewska K, Jonczyk K, Modlinska-Cwalinska A. et al. Visceral larva migrans syndrome: analysis of serum cytokine levels in children with hepatic lesions confirmed in radiological findings. Parasite Immunol 2014; 36: 668-673
68 Sanchez SS, Garcia HH, Nicoletti A. Clinical and magnetic resonance imaging findings of neurotoxocariasis. Front Neurol 2018; 9: 53
69 Deshayes S, Bonhomme J, de La Blanchardiere A. Neurotoxocariasis: a systematic literature review. Infection 2016; 44: 565-574
70 Morais FB, Maciel AL, Arantes TE. et al. Ultrasonographic findings in ocular toxocariasis. Arq Bras Oftalmol 2012; 75: 43-47
71 Kang YR, Kim SA, Jeon K. et al. Toxocariasis as a cause of new pulmonary infiltrates. Int J Tuberc Lung Dis 2013; 17: 412-417
72 Yoon YS, Lee CH, Kang YA. et al. Impact of toxocariasis in patients with unexplained patchy pulmonary infiltrate in Korea. J Korean Med Sci 2009; 24: 40-45
73 Hur JH, Lee IJ, Kim JH. et al. Chest CT findings of toxocariasis: correlation with laboratory results. Clin Radiol 2014; 69: e285-e290
74 Shrand H. Visceral larva migrans. Toxocara canis infection. Lancet 1964; 1: 1357-1359
75 Ota KV, Dimaras H, Heon E. et al. Toxocariasis mimicking liver, lung, and spinal cord metastases from retinoblastoma. Pediatr Infect Dis J 2009; 28: 252-254
76 Anderson A, Fordham LA, Bula ML. et al. Visceral larval migrans masquerading as metastatic disease in a toddler with Wilms tumor. Pediatr Radiol 2006; 36: 265-267
77 Beshear JR, Hendley JO. Severe pulmonary involvement in visceral larva migrans. Am J Dis Child 1973; 125: 599-600
78 Lee KH, Kim TJ, Lee KW. Pulmonary toxocariasis: initial and follow-up CT findings in 63 patients. Am J Roentgenol 2015; 204: 1203-1211
79 Schantz PM, Glickman LT. Toxocaral visceral larva migrans. N Engl J Med 1978; 298: 436-439
80 Magnaval JF, Glickman LT, Dorchies P. et al. Highlights of human toxocariasis. Korean J Parasitol 2001; 39: 1-11
81 Elefant GR, Shimizu SH, Sanchez MC. et al. A serological follow-up of toxocariasis patients after chemotherapy based on the detection of IgG, IgA, and IgE antibodies by enzyme-linked immunosorbent assay. J Clin Lab Anal 2006; 20: 164-172
82 Sturchler D, Schubarth P, Gualzata M. et al. Thiabendazole vs. albendazole in treatment of toxocariasis: a clinical trial. Ann Trop Med Parasitol 1989; 83: 473-478
83 Drugs for Parasitic Infections, 3rd ed. The Medical Letter. NY; 2013
84 Magnaval JF. Comparative efficacy of diethylcarbamazine and mebendazole for the treatment of human toxocariasis. Parasitology 1995; 110: 529-533
85 Bhatia V, Sarin SK. Hepatic visceral larva migrans: evolution of the lesion, diagnosis, and role of high-dose albendazole therapy. Am J Gastroenterol 1994; 89: 624-627
86 Barisani-Asenbauer T, Maca SM, Hauff W. et al. Treatment of ocular toxocariasis with albendazole. J Ocul Pharmacol Ther 2001; 17: 287-294
87 Small KW, McCuen 2nd BW, de Juan Jr E. et al. Surgical management of retinal traction caused by toxocariasis. Am J Ophthalmol 1989; 108: 10-14
88 Giuliari GP, Ramirez G, Cortez RT. Surgical treatment of ocular toxocariasis: anatomic and functional results in 45 patients. Eur J Ophthalmol 2011; 21: 490-494