Abstract
Purpose
Radiotherapy showed the potential to effectively kill the cysts of pulmonary cystic echinococcosis (CE). However, little is known about its safety. This study was designed to investigate the safety of three-dimensional conformal radiotherapy (3D-CRT) on the normal lung tissue adjacent to the cyst and blood of sheep naturally infected with pulmonary CE.
Methods
Twenty pulmonary CE sheep were randomly divided into control group (n = 5) and radiation groups with a dose of 30 Gray (Gy) (n = 5), 45 Gy (n = 5), and 60 Gy (n = 5), respectively. Animals in control group received no radiation. Heat shock protein 70 (Hsp70), tumor growth factor-β (TGF-β), matrix metalloproteinase-2 (MMP-2) and MMP-9 in the lung tissues adjacent to the cysts, which were considered to be closely related to the pathogenesis of CE, were evaluated after 3D-CRT. A routine blood test was conducted.
Results
The results showed that there were multiple cysts of various sizes with protoscoleces in the lung tissues of sheep, and necrotic cysts were found after 3D-CRT. 3D-CRT significantly increased the mRNA level of Hsp70, enhanced the protein level of TGF-β and slightly increased the expression of MMP-2 and MMP-9 in lung tissues adjacent to the cysts. 3D-CRT did not significantly alter the amount of WBC, HB and PLT in sheep blood.
Conclusions
The results suggested that 3D-CRT may suppress the inflammation and induce less damage of the normal lung tissues and blood. We preliminarily showed that 3D-CRT under a safe dose may be used to treat pulmonary CE.
Similar content being viewed by others
Data Availability
The data sets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
McManus DP, Gray DJ, Zhang W, Yang Y (2012) Diagnosis, treatment, and management of echinococcosis. BMJ 344:e3866. https://doi.org/10.1136/bmj.e3866
Cadavid Restrepo AM, Yang YR, McManus DP, Gray DJ, Giraudoux P, Barnes TS et al (2016) The landscape epidemiology of echinococcoses. Infect Dis Poverty 5:13. https://doi.org/10.1186/s40249-016-0109-x
Lashkarizadeh MR, Hooshmand N, Nasibi S, Mohammadi MA, Shamsaddini S, Kamyabi H et al (2019) Genetic profile of hydatid cysts in patients with multi-organ involvement: mixed infections by different strains. Vector Borne Zoonotic Dis 19(10):724–730. https://doi.org/10.1089/vbz.2018.2427
Ding NH, Li JJ, Sun LQ (2013) Molecular mechanisms and treatment of radiation-induced lung fibrosis. Curr Drug Targets 14(11):1347–1356. https://doi.org/10.2174/13894501113149990198
Ozdol C, Yildirim AE, Daglioglu E, Divanlioglu D, Erdem E, Belen D (2011) Alveolar hydatid cyst mimicking cerebellar metastatic tumor. Surg Neurol Int 2:13. https://doi.org/10.4103/2152-7806.76281
Dominique R, Francesca T, Renato U, Silivia B, Amedea M, Silvio Q (2002) Terpyridine Zn (II), Ru (III) and Ir (III) complexex as new asymmetric chromophores for nonlinear optics: first evidence for a shift from positive to negative value of the quadratic hyperpolarizability of a ligand carrying an electron donor substituent upon coordination to different metal centres. Chem Commun (Camb) 8:846–847. https://doi.org/10.1039/b201221a
Aasen TD, Nasrollah L, Seetharam A (2018) Drug-induced liver failure requiring liver transplant: report and review of the role of albendazole in managing echinococcal infection. Exp Clin Transplant 16(3):344–347. https://doi.org/10.6002/ect.2015.0313
Engels E, Li N, Davis J, Paino J, Cameron M, Dipuglia A et al (2020) Toward personalized synchrotron microbeam radiation therapy. Sci Rep 10(1):8833. https://doi.org/10.1038/s41598-020-65729-z
Mao R, Wu G, Wang H, Lu P, Li J, Li H et al (2017) Effects of X-ray on the metacestodes of Echinococcus granulosus in vitro. BMC Infect Dis 17(1):636. https://doi.org/10.1186/s12879-017-2741-x
Zhang Y, Lu P, Qi H, Wu G, Mao R, Bao Y (2021) Radiotherapy for the treatment of pulmonary hydatidosis in sheep. Open Life Sci 16(1):1405–1411. https://doi.org/10.1515/biol-2021-0139
Zhang YF, Xie ZR, Ni YQ, Mao R, Qi HZ, Yang YG et al (2011) Curative effect of radiotherapy at various doses on subcutaneous alveolar echinococcosis in rats. Chin Med J (Engl) 124(18):2845–2848
Fernández-Fernández MR, Valpuesta JM (2018) Hsp70 chaperone: a master player in protein homeostasis. F1000Res. https://doi.org/10.12688/f1000research.15528.1
Ortona E, Margutti P, Delunardo F, Vaccari S, Riganò R, Profumo E et al (2003) Molecular and immunological characterization of the C-terminal region of a new Echinococcus granulosus Heat Shock Protein 70. Parasite Immunol 25(3):119–126. https://doi.org/10.1046/j.1365-3024.2003.00617.x
Meng XM, Nikolic-Paterson DJ, Lan HY (2016) TGF-β: the master regulator of fibrosis. Nat Rev Nephrol 12(6):325–338. https://doi.org/10.1038/nrneph.2016.48
Batlle E, Massagué J (2019) Transforming growth factor-β signaling in immunity and cancer. Immunity 50(4):924–940. https://doi.org/10.1016/j.immuni.2019.03.024
Díaz Á (2017) Immunology of cystic echinococcosis (hydatid disease). Br Med Bull 124(1):121–133. https://doi.org/10.1093/bmb/ldx033
Mirzavand S, Rafiei A, Teimoori A, Khorsandi L, Bahreini A, Motamedfar A et al (2020) Gene expression in human liver fibrosis associated with Echinococcus granulosus sensu lato. Parasitol Res 119(7):2177–2187. https://doi.org/10.1007/s00436-020-06700-9
Sokouti M, Sokouti M, Sokouti B (2001) Structure of the pulmonary hydatid cyst. J Med Ultrason 41(2):251–252. https://doi.org/10.1007/s10396-013-0492-x
Kim JY, Choeng HC, Ahn C, Cho SH (2009) Early and late changes of MMP-2 and MMP-9 in bleomycin-induced pulmonary fibrosis. Yonsei Med J 50(1):68–77. https://doi.org/10.3349/ymj.2009.50.1.68
Corbel M, Belleguic C, Boichot E, Lagente V (2002) Involvement of gelatinases (MMP-2 and MMP-9) in the development of airway inflammation and pulmonary fibrosis. Cell Biol Toxicol 18(1):51–61. https://doi.org/10.1023/a:1014471213371
Marco M, Baz A, Fernandez C, Gonzalez G, Hellman U, Salinas G et al (2006) A relevant enzyme in granulomatous reaction, active matrix metalloproteinase-9, found in bovine Echinococcus granulosus hydatid cyst wall and fluid. Parasitol Res 100(1):131–139. https://doi.org/10.1007/s00436-006-0237-5
Funding
This study was supported by the National Natural Science Foundation (Nos. 81860556 and 81860360) and the State Key Laboratory and the High Incidence Disease of Central Asia (SKL-HIDCA-2019-29).
Author information
Authors and Affiliations
Contributions
Data curation: ZYF, LPF and QHZ; funding acquisition: MR, QHZ and ZYF; conceptualization: MR and BYX; writing—original draft: ZYF and LPF; writing—review and editing: MR and BYX. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflicts of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Ethics approval
The study protocols were approved by the Ethics Committee of the First Affiliated Hospital of Xinjiang Medical University (approval No. IACUC-2014021002).
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, Y., Lu, P., Qi, H. et al. Safety of Three-Dimensional Conformal Radiotherapy on the Sheep with Pulmonary Cystic Echinococcosis: A Preliminary Study. Acta Parasit. 69, 559–566 (2024). https://doi.org/10.1007/s11686-023-00751-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11686-023-00751-5