Skip to main content
Log in

The damages of high intensity focused ultrasound to transplanted hydatid cysts in abdominal cavities of rabbits with aids of ultrasound contrast agent and superabsorbent polymer

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The present study investigates the damages of high intensity focused ultrasound (HIFU) to transplanted hydatid cysts in abdominal cavities of rabbits with aids of ultrasound contrast agent (UCA) and superabsorbent polymer (SAP) alone or in combination. A rabbit model with transplanted hydatid cyst was established by implanting hydatid cyst isolated from infected sheep liver, and HIFU was used to ablate the transplanted cysts with the aid of UCA and SAP alone or in combination. The hydatid cyst with thin wall, good elasticity, approximately spherical, and a diameter of approximately 30 mm was selected for the following experiments. According to our previous studies, a mixture of 0.1 g SAP and 0.5 ml anhydrous ethanol, and the solution of 0.1 ml UCA SonoVue, or both materials were injected into different cyst before HIFU ablation, respectively. The cyst inoculated with the SAP and UCA alone or in combination was immediately implanted into the abdominal cavity of rabbit for HIFU ablation at a dosage of 100 W acoustic powers. The ablation mode was spot scanning at the speed of 3 mm/s. Every target point was scanned three times; every ablating time lasted 3 s. The distance of each ablated layer was 5 mm. The total ablation time depended on the volume of cyst. The comparison of ultrasound image for each layer of hydatid cyst was made before and after HIFU ablation. The protoscolices in ablated cysts were stained by trypan blue exclusion assay, and their structures were observed by light microscopy. To estimate ablation effects of HIFU to the walls of hydatid cysts, the ultrastructure changes of cyst walls were examined by electron microscopy. The pathological changes of rabbits’ skins through which ultrasound penetrated were observed to investigate the side effects of HIFU ablation. The results demonstrated that HIFU had some lethal effects to hydatid cysts in vivo, namely, echo enhancements of ultrasound images of cysts, increases in mortality rate of protoscolices from 15.19 % (HIFU alone) to 48.66 % (HIFU + SAP), 38.67 % (HIFU + UCA), and 67.75 % (HIFU + SAP + UCA), respectively, serious structural damages of protoscolices, and destructions or even disappearance of laminated layers and germinal layers in the walls of hydatid cysts ablated by HIFU aided with UCA and SAP alone or in combination. This study demonstrated that destructive effects of HIFU to transplanted hydatid cyst could be enhanced by UCA and SAP alone, but the destruction of HIFU aided with a combination of UCA and SAP to hydatid cysts was more effective than those aided with UCA or SAP alone. The enhanced thermal and cavitation effects of HIFU induced by UCA and SAP might be involved in the enhanced destructive effects of HIFU on hydatid cysts. There were no evidences of pathological changes on rabbits’ skins overlying the hydatid cysts after HIFU ablation. The results suggested that the rabbit model with transplanted hydatid cyst may serve as an optional animal model for the experiments of HIFU ablation to hydatid cyst in vivo, and the materials of UCA and SAP were proved as enhancing agents of HIFU ablation to hydatid cysts, and HIFU at a dosage of 100 W acoustic powers was a safe and feasible parameter to ablate the hydatid cysts in this special animal model. These results laid a theoretical foundation for improving HIFU therapy for cystic echinococcosis by inoculation of UCA and SAP into hydatid cysts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16

Similar content being viewed by others

References

  • Addy F, Alakonya A, Wamae N, Magambo J, Mbae C, Mulinge E, Zeyhle E, Wassermann M, Kern P, Romig T (2012) Prevalence and diversity of cystic echinococcosis in livestock in Maasailand, Kenya. Parasitol Res 111(6):2289–2294

    Article  PubMed  Google Scholar 

  • Araj GF, Matossian RM, Frayha GJ (1977) The host response in secondary hydatidosis of mice. I. Circulating antibodies. Parasitol Res 52(1):23–30

    CAS  Google Scholar 

  • Borden MA, Qin S, Ferrara KW (2010) Ultrasound contrast agents. In: Weissleder R (ed) Molecular imaging. BC Decker, Hamilton, pp 425–444

  • Brunetti E, Junghanss T (2009) Update on cystic hydatid disease. Curr Opin Infect Dis 22(5):497–502

    Article  PubMed  Google Scholar 

  • Brunetti E, Kern P, Vuitton DA (2010) Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114(1):1–16

    Article  PubMed  Google Scholar 

  • Cai H, Chen LL, Ye B, Liu AB, Zhang J, Zhao YF (2013) The destructive effects of high-intensity focused ultrasound on hydatid cysts enhanced by ultrasound contrast agent and superabsorbent polymer alone or in combination. Parasitol Res 112:707–717. doi:10.1007/s00436-00012-03191-00434

    Article  PubMed  Google Scholar 

  • Cheung TT, Chu FS, Jenkins CR, Tsang DS, Chok KS, Chan AC, Yau TC, Chan SC, Poon RTP, Lo CM, Fan ST (2012) Tolerance of high-intensity focused ultrasound ablation in patients with hepatocellular carcinoma. World J Surg 36(10):2420–2427

    Article  PubMed  Google Scholar 

  • Deplazes P, Gottstein B, Eckert J, Jenkins DJ, Ewald D, Jimenez-Palacios S (1992) Detection of Echinococcus coproantigens by enzyme-linked immunosorbent assay in dogs, dingoes and foxes. Parasitol Res 78(4):303–308

    Article  PubMed  CAS  Google Scholar 

  • Eckert J, Thompson RCA, Lymbery AJ, Pawlowski ZS, Gottstein B, Morgan UM (1993) Further evidence for the occurrence of a distinct strain of Echinococcus granulosus in European pigs. Parasitol Res 79(1):42–48

    Article  PubMed  CAS  Google Scholar 

  • Eckert J, Thompson RCA, Michael SA, Kumaratilake LM, El-Sawah HM (1989) Echinococcus granulosus of camel origin: development in dogs and parasite morphology. Parasitol Res 75(7):536–544

    Article  PubMed  CAS  Google Scholar 

  • Ferragut G, Nieto A (1996) Antibody response of Echinococcus granulosus infected mice: recognition of glucidic and peptidic epitopes and lack of avidity maturation. Parasite Immunol 18(8):393–402

    Article  PubMed  CAS  Google Scholar 

  • Golemanov B, Grigorov N, Mitova R, Genov J, Vuchev D, Tamarozzi F, Brunetti E (2011) Efficacy and safety of PAIR for cystic echinococcosis: experience on a large series of patients from Bulgaria. AmJTrop Med Hyg 84(1):48–51

    Article  Google Scholar 

  • Gottstein B, Eckert J, Fey H (1983) Serological differentiation between Echinococcus granulosus and E. multilocularis infections in man. Parasitol Res 69(3):347–356

    CAS  Google Scholar 

  • Gottstein B, Eckert J, Michael SA, Thompson RCA (1987) Echinococcus granulosus antigens: immunoelectrophoretic and Western blot analysis of hydatid cyst fluids. Parasitol Res 73(2):186–189

    Article  PubMed  CAS  Google Scholar 

  • Gottstein B, Eckert J, Woodtli W (1984) Determination of parasite-specific immunoglobulins using the ELISA in patients with echinococcosis treated with mebendazole. Parasitol Res 70(3):385–389

    Article  CAS  Google Scholar 

  • He W, Wang W, Zhou P, Wang YX, Zhou P, Li RZ, Wang JS, Ahuja AT (2011) Enhanced ablation of high intensity focused ultrasound with microbubbles: an experimental study on rabbit hepatic VX2 tumors. Cardiovasc Intervent Radiol 34(5):1050–1057

    Article  PubMed  CAS  Google Scholar 

  • Hemphill A, Muller J (2009) Alveolar and cystic echinococcosis: towards novel chemotherapeutical treatment options. J Helminthol 83(2):99–111

    Article  PubMed  CAS  Google Scholar 

  • Janssen D, Osuna A, Lazuen J, De Rycke PH (1992) Comparative cytotoxicity of secondary hydatid cysts, protoscoleces, and in vitro developed microcysts of Echinococcus granulosus. J Helminthol 66(2):124–131

    Article  PubMed  CAS  Google Scholar 

  • Jenkins DJ, Romig T, Thompson RC (2005) Emergence/re-emergence of Echinococcus spp.—a global update. Int J Parasitol 35(11–12):1205–1219

    Article  PubMed  CAS  Google Scholar 

  • Kong J, Ye B, Zhang J, Han XM, Yang YH, Li FQ (2011) Effect of high intensity focused ultrasound on Echinococcus granulosus protoscolices with the aid of microbubble contrast agent. Chin J Zoon 27(8):687–691

    Google Scholar 

  • Li Q, Du J, Yu M, He G, Luo W, Li H, Zhou X (2009) Transmission electron microscopy of VX2 liver tumors after high-intensity focused ultrasound ablation enhanced with SonoVue. Adv Ther 26(1):117–125

    Article  PubMed  Google Scholar 

  • Luo W, Zhou X, Yu M, He G, Zheng X, Li Q, Liu Q, Han Z, Zhang J, Qian Y (2009) Ablation of high-intensity focused ultrasound assisted with SonoVue on rabbit VX2 liver tumors: sequential findings with histopathology, immunohistochemistry, and enzyme histochemistry. Ann Surg Oncol 16(8):2359–2368

    Article  PubMed  Google Scholar 

  • Mamuti W, Yamasaki H, Sako Y, Nakaya K, Nakao M, Lightowlers MW, Ito A (2002) Usefulness of hydatid cyst fluid of Echinococcus granulosus developed in mice with secondary infection for serodiagnosis of cystic echinococcosis in humans. Clin Diagn Lab Immunol 9(3):573–576

    PubMed  Google Scholar 

  • McManus DP, Zhang W, Li J, Bartley PB (2003) Echinococcosis. Lancet 362(9392):1295–1304

    Article  PubMed  Google Scholar 

  • Moazeni M, Larki S (2010) In vitro effectiveness of acidic and alkline solutions on scolices of hydatid cyst. Parasitol Res 106(4):853–856

    Article  PubMed  Google Scholar 

  • Payne L, Fitchett JR (2010) Bringing neglected tropical diseases into the spotlight. Trends Parasitol 26(9):421–423

    Article  PubMed  Google Scholar 

  • Richter J, Orhun A, Grüner B, Müller-Stöver I, Reuter S, Romig T, Häussinger D, Kern P (2009) Autochthonous cystic echinococcosis in patients who grew up in Germany. Euro Surveill 14(22):pii:19229

    Google Scholar 

  • Robbin ML (2001) Ultrasound contrast agents: a promising future. Radiol Clin N Am 39(3):399–414

    Article  PubMed  CAS  Google Scholar 

  • Rogan MT (1998) T-cell activity associated with secondary infections and implanted cysts of Echinococcus granulosus in BALB/c mice. Parasite Immunol 20(11):527–533

    Article  PubMed  CAS  Google Scholar 

  • Romig T, Omer RA, Zeyhle E, Hüttner M, Dinkel A, Siefert L, Elmahdi IE, Magambo J, Ocaido M, Menezes CN, Ahmed ME, Mbae C, Grobusch MP, Kern P (2011) Echinococcosis in sub-Saharan Africa: emerging complexity. Vet Parasitol 181(1):43–47

    Article  PubMed  CAS  Google Scholar 

  • Ryan P, Finelli A, Lawrentschuk N, Fleshner N, Sweet J, Cheung C, van der Kwast T, Evans A (2012) Prostatic needle biopsies following primary high intensity focused ultrasound (HIFU) therapy for prostatic adenocarcinoma: histopathological features in tumour and non-tumour tissue. J Clin Pathol 65(8):729–734

    Article  PubMed  Google Scholar 

  • Saimot AG (2001) Medical treatment of liver hydatidosis. World J Surg 25(1):15–20

    Article  PubMed  CAS  Google Scholar 

  • Stojkovic M, Zwahlen M, Teggi A, Vutova K, Cretu CM, Virdone R, Nicolaidou P, Cobanoglu N, Junghanss T (2009) Treatment response of cystic echinococcosis to benzimidazoles: a systematic review. PLoS Negl Trop Dis 3(9):e524

    Article  PubMed  Google Scholar 

  • Sun Y, Zheng Y, Ran H, Zhou Y, Shen H, Chen Y, Chen H, Krupka TM, Li A, Li P (2012) Superparamagnetic PLGA-iron oxide microcapsules for dual-modality US/MR imaging and high intensity focused US breast cancer ablation. Biomaterials 33(24):5854–5864

    Article  PubMed  CAS  Google Scholar 

  • Tung YS, Liu HL, Wu CC, Ju KC, Chen WS, Lin WL (2006) Contrast-agent-enhanced ultrasound thermal ablation. Ultrasound Med Biol 32(7):1103–1110

    Article  PubMed  Google Scholar 

  • Varcasia A, Garippa G, Pipia AP, Scala A, Brianti E, Giannetto S, Battelli G, Poglayen G, Micagni G (2008) Cystic echinococcosis in equids in Italy. Parasitol Res 102(4):815–818

    Article  PubMed  CAS  Google Scholar 

  • Wang JA, Zou XY, Ye B, Zhang CW, Zhao FS (2007a) Pathological change in hydatid cysts of Echinococcus granulosus treated with high intensity focused ultrasound. Chin J Parasitol Parasit Dis 25(6):462–465

    Google Scholar 

  • Wang JA, Zou XY, Ye B, Zhang CW, Zhao FS, Han XM, Li FQ, Zou JZ (2009) High intensity focus ultrasound kills hydatid cysts of Echinococcus granulosus. Acta Acad Med Mil Tert 31(14):1333–1336

    CAS  Google Scholar 

  • Wang JA, Zou XY, Ye B, Zhang CW, Zhao FS, Han XM, Yang YH, Li FQ (2007b) The heat effect of irradiation with high intensity focused ultrasound on the hydatid cysts of Echinococcus granulosus. Chin J Zoon 23(6):576–579

    Google Scholar 

  • Wang W, Wang Y, Wang T, Wang J, Wang L, Tang J (2012) Safety and efficacy of US-guided high-intensity focused ultrasound for treatment of submucosal fibroids. Eur Radiol 22(11):2553–2558

    Article  PubMed  Google Scholar 

  • Yang FY, Chen CC, Horng SC, Chiu WH, Yeh CF (2012) Microbubble-enhanced functional changes in arteries induced by pulsed high-intensity focused ultrasound exposure. Med Eng Phys 34(3):313–317

    Article  PubMed  Google Scholar 

  • Zderic V, Brayman AA, Sharar SR, Crum LA, Vaezy S (2006) Microbubble-enhanced hemorrhage control using high intensity focused ultrasound. Ultrasonics 45(1–4):113–120

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Kong J, Ye B, Zou XY, Wu WH (2011a) Preparation and water absorptive properties of starch based super absorbent resin for hydatid fluid. Chin J Zoon 27(12):1090–1093

    Google Scholar 

  • Zhang J, Ye B, Kong J, Cai H, Zhao YF, Han XM, Li FQ (2013) In vitro protoscolicidal effects of high-intensity focused ultrasound enhanced by a superabsorbent polymer. Parasitol Res 112:385–391. doi:10.1007/s00436-00012-03176-00433

    Article  PubMed  Google Scholar 

  • Zhang J, Ye B, Zou XY, Wu WH, Han XM (2011b) Establishment of laboratory animal models of hydatid disease through inoculating mice and rabbits with echinococcus granulosus protoscolices. Acta Acad Med Mil Tert 33(7):679–681

    Google Scholar 

  • Zhang J, Ye B, Zou XY, Wu WH, Li FQ, Gong XB, Han XM (2007) Morphological changes of hydatids of Echinococcus granulosus in mice treated by high intensity focused ultrasound. Chin J Zoon 23(12):1187–1190

    Article  Google Scholar 

  • Zou XY, Wang JA, Zhao HL, Zhang J, Wu WH, Ye B (2009) Echinococcus granulosus: protoscolicidal effect of high intensity focused ultrasound. Exp Parasitol 121(4):312–316

    Article  PubMed  Google Scholar 

  • Zou XY, Ye B, Wang JA, Zhang CW, Han XM, Li FQ (2007) Effects of HIFU on hydatid cysts of Echinococcus granulosus: two exposure pattern comparison. Chin J Ultrasound Med 23(8):574–577

    Google Scholar 

Download references

Acknowledgments

This study was funded by the Nation al Natural Science Foundation of China (numbers 30972567 and 30371258). The authors appreciate the assistance of HIFU Therapeutic Center, the Affiliated Hospital of Qinghai University, and are grateful to Mr. Hailong Zhao in Department of Pathogenic Biology, Medical College, Qinghai University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bin Ye.

Additional information

This project was supported by the National Natural Science Foundation of China (No. 30972567 and No.30371258).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, AB., Cai, H., Ye, B. et al. The damages of high intensity focused ultrasound to transplanted hydatid cysts in abdominal cavities of rabbits with aids of ultrasound contrast agent and superabsorbent polymer. Parasitol Res 112, 1865–1875 (2013). https://doi.org/10.1007/s00436-013-3340-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3340-4

Keywords

Navigation