Carbogen gas-challenge BOLD fMRI in assessment of liver hypoxia after portal microcapsules implantation


Autoři: Yuefu Zhan aff001;  Yehua Wu aff002;  Jianqiang Chen aff003
Působiště autorů: Department of Radiology, Maternal and Child Health Hospital of Hainan Province, Haikou, Hainan, China aff001;  Hainan General Hospital, Haikou, China aff002;  Department of Radiology, Xiangya School of Medicine Affiliated Haikou Hospital, Central South University, Haikou, Hainan, China aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225665

Souhrn

Background

Hypoxia is one of the key factors affecting the survival of islet cells transplanted via the portal vein. Blood oxygen level dependent functional magnetic resonance imaging (BOLD-fMRI) is the only imaging technique that can detect the level of blood oxygen level in vivo. However, so far no study has indicated that BOLD-fMRI can be applied to monitor the liver oxygen level after islet transplantation.

Objective

To evaluate the value of Carbogen-challenge BOLD MRI in assessing the level of hypoxia in liver tissue after portal microcapsules implanted.

Methods

Fifty-one New Zealand rabbits were randomly divided into three experimental groups (15 in each group) were transplanted microencapsulated 1000 microbeads/kg (PV1 group), 3000 microbeads/kg (PV2 group), 5000 microbeads/kg (PV3 group), and 6 rabbits were injected with the same amount of saline as the control group, BOLD-fMRI was performed following carbogen breathing in each group after transplantation on 1d, 2d, 3d and 7d, T2* weighted image, R2* value and ΔR2* value parameters for the liver tissue. Pathological examinations including liver gross pathology, H&E staining and pimonidazole immunohistochemistry were performed after BOLD-fMRI. The differences of pathological results among each group were compared. The ΔR2* values and transplanted doses were analyzed.

Results and conclusions

ΔR2* values at the 1-3d and 7d after transplantation were significantly different in each groups (P<0.05). ΔR2* values decreased gradually with the increase of transplanted dose, and was negatively correlated with transplant dose at 3d after transplantation (r = -0.929, P <0.001). Liver histopathological examination showed that the degree of hypoxia of liver tissue increased with the increase of transplanted doses, Carbogen-challenge BOLD-fMRI can assess the degree of liver hypoxia after portal microcapsules implanted, which provided a monitoring method for early intervention.

Klíčová slova:

Hemodynamics – Hepatocytes – Hypoxia – Liver transplantation – Medical hypoxia – Oxygen – Portal veins – Islet transplantation


Zdroje

1. Shapiro AMJ, Ricordi C, Hering BJ, Auchincloss H, Lindblad R, Robertson RP, et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med, 2006, 355(13): 1318–1330. doi: 10.1056/NEJMoa061267 17005949

2. Bruni A, Gala-Lopez B, Pepper AR, Abualhassan NS, Shapiro AJ. Islet cell transplantation for the treatment of type 1 diabetes: recent advances and future challenges. Diabetes Metab Syndr Obes, 2014, 7: 211. doi: 10.2147/DMSO.S50789 25018643

3. Pepper AR, Gala-Lopez B, Pawlick R, Merani S, Kin T, Shapiro AM. A prevascularized subcutaneous device-less site for islet and cellular transplantation. Nat Biotechnol, 2015, 33(5): 518–523. doi: 10.1038/nbt.3211 25893782

4. Lablanche S, Borot S, Wojtusciszyn A, Bayle F, Tétaz R, Badet L, et al. Five-year metabolic, functional, and safety results of patients with type 1 diabetes transplanted with allogenic islets within the Swiss-French GRAGIL network. Diabetes Care, 2015, 38(9): 1714–1722. doi: 10.2337/dc15-0094 26068866

5. Brennan DC, Kopetskie HA, Sayre PH, Alejandro R, Cagliero E, Shapiro AM, et al. Long-Term Follow-Up of the Edmonton Protocol of Islet Transplantation in the United States. Am J Transplant, 2016, 16(2): 509–517. doi: 10.1111/ajt.13458 26433206

6. Yang HK, Yoon KH. Current status of encapsulated islet transplantation. J Diabetes Complications, 2015, 29(5): 737–743. doi: 10.1016/j.jdiacomp.2015.03.017 25881917

7. Foster GA, García AJ. Bio-synthetic material for immunomodulation of islet transplants. Adv Drug Deliver Rev, 2017, 114: 266–271.

8. Tomei AA, Manzoli V, Fraker CA, Giraldo J, Velluto D, Najjar M, et al. Device design and materials optimization of conformal coating for islets of Langerhans. Proc Natl Acad Sci USA, 2014, 111(29):10514–10519. doi: 10.1073/pnas.1402216111 24982192

9. Osama Gaber A, Chamsuddin A, Fraga D, Fisher J, Lo A. Insulin independence achieved using the transmesenteri approach to the portal vein for islet transplantation. Transplantation, 2004, 77 (2): 309–311. doi: 10.1097/01.TP.0000101509.35249.A0 14742999

10. Froud T, Ricordi C, Baidal DA, Hafiz MM, Ponte G, Cure P, et al. Islet transplantation in type 1 diabetes mellitus using cultured islets and steroid-free immunosuppression: Miami experience. Am J Transplant, 2005, 5(8): 2037–2046. doi: 10.1111/j.1600-6143.2005.00957.x 15996257

11. Rother KI, Harlan DM. Challenges facing islet transplantation for the treatment of type 1 diabetes mellitus. J Clin Invest, 2004, 114(7): 877. doi: 10.1172/JCI23235 15467822

12. Wilhelm JJ, Bellin MD, Dunn TB, Balamurugan AN, Pruett TL, Radosevich DM, et al. Proposed thresholds for pancreatic tissue-volume for safe intraportal islet autotransplantation after total-pancreatectomy. Am J Transplant, 2013, 13(12):3183–3191. doi: 10.1111/ajt.12482 24148548

13. Ullsten S, Lau J, Carlsson PO. Vascular heterogeneity between native rat pancreatic islets is responsible for differences in survival and revascularisation post transplantation. Diabetologia, 2015, 58(1): 132–139. doi: 10.1007/s00125-014-3385-7 25257098

14. Emamaullee JA, Shapiro AM. Factors Influencing the Loss of Cell Mass in Islet Transplantation. Cell transplant, 2007, 16(1): 1–8.

15. Ullsten S, Lau J, Carlsson PO. Vascular heterogeneity between native rat pancreatic islets is responsible for differences in survival and revascularisation post transplantation. Diabetologia, 2015, 58(1): 132–139. doi: 10.1007/s00125-014-3385-7 25257098

16. Christen T, Bolar DS, Zaharchuk G. Imaging brain oxygenation with MRI using blood oxygenation approaches: methods, validation, and clinical applications. AJNR Am J Neuroradiol, 2013, 34(6): 1113–1123. doi: 10.3174/ajnr.A3070 22859287

17. Barash H, Gross E, Edrei Y, Pappo O, Spira G, Vlodavsky I, et al. Functional magnetic resonance imaging monitoring of pathological changes in rodent livers during hyperoxia and hypercapnia. Hepatology, 2008, 48(4): 1232–1241. doi: 10.1002/hep.22394 18629804

18. Luo J, Abaci Turk E, Bibbo C, Gagoski B, Roberts DJ, Vangel M, et al. In Vivo Quantification of Placental Insufficiency by BOLD MRI: A Human Study. Sci Rep-UK, 2017, 7(1): 3713.

19. Schoennagel BP, Yamamura J, Fischer R, Tavares de Sousa M, Weyhmiller M, Birkelbach M, et al. BOLD MRI in the brain of fetal sheep at 3T during experimental hypoxia. J Magn Reson Imaging, 2015, 41(1): 110–116. doi: 10.1002/jmri.24555 24357078

20. Nordsmark M, Loncaster J, Aquino-Parsons C, Chou SC, Ladekarl M, Havsteen H, et al. Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas. Radiother Oncol, 2003, 67(1):35–44. doi: 10.1016/s0167-8140(03)00010-0 12758238

21. Lim F, Sun AM. Microencapsulated islets as bioartificial endocrine pancreas. Science. 1980 21;210(4472):908–910. doi: 10.1126/science.6776628 6776628

22. Brissova M, Fowler M, Wiebe P, Shostak A, Shiota M, Radhika A, et al. Intraislet endothelial cells contribute to revascularization of transplanted pancreatic islets. Diabetes, 2004, 53(5): 1318–1325. doi: 10.2337/diabetes.53.5.1318 15111502

23. Suszynski TM, Avgoustiniatos ES, Papas KK. Oxygenation of the Intraportally transplanted pancreatic islet. J Diabetes Res. 2016; 2016:7625947. doi: 10.1155/2016/7625947 27872862

24. Rodriguez-Brotons A, Bietiger W, Peronet C, Magisson J, Sookhareea C, Langlois A, et al. Impact of pancreatic rat islet density on cell survival during hypoxia. J Diabetes Res, 2016, 2016(22):1–10.

25. Sakata N, Hayes P, Tan A, Chan NK, Mace J, Peverini R, et al. MRI assessment of ischemic liver after intraportal islet transplantation. Transplantation, 2009, 87(6):825–830. doi: 10.1097/TP.0b013e318199c7d2 19300184

26. Davalli AM, Scaglia L, Zangen DH, Hollister J, Bonner-Weir S, Weir GC. Vulnerability of islets in the immediate posttransplantation period. Dynamic changes in structure and function. Diabetes, 1996, 45(9):1161–1167. doi: 10.2337/diab.45.9.1161 8772716

27. Kaanders JH, Wijffels KI, Marres HA, Ljungkvist AS, Pop LA, van den Hoogen FJ, et al. Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Res, 2002, 62(23): 7066–7074. 12460928

28. King AL, Mantena SK, Andringa KK, Millender-Swain T, Dunham-Snary KJ, Oliva CR, et al. The methyl donor S-adenosylmethionine prevents liver hypoxia and dysregulation of mitochondrial bioenergetic function in a rat model of alcohol-induced fatty liver disease. Redox Biol, 2016, 9: 188–197. doi: 10.1016/j.redox.2016.08.005 27566282

29. Ragnum HB, Vlatkovic L, Lie AK, Axcrona K, Julin CH, Frikstad KM, et al. The tumour hypoxia marker pimonidazole reflects a transcriptional programme associated with aggressive prostate cancer. Brit J Cancer, 2015, 112(2): 382–390. doi: 10.1038/bjc.2014.604 25461803

30. Choi JW, Kim H, Kim HC, Lee Y, Kwon J, Yoo RE, et al. Blood oxygen level-dependent MRI for evaluation of early response of liver tumors to chemoembolization: an animal study. Anticancer Res, 2013, 33(5): 1887–1892. 23645735

31. Jin N, Deng J, Chadashvili T, Zhang Y, Guo Y, Zhang Z, et al. Carbogen Gas–Challenge BOLD MR Imaging in a Rat Model of Diethylnitrosamine-induced Liver Fibrosis. Radiology, 2010, 254(1): 129–137. doi: 10.1148/radiol.09090410 20032147

32. Patterson AJ, Priest AN, Bowden DJ, Wallace TE, Patterson I, Graves MJ, et al. Quantitative BOLD imaging at 3T: Temporal changes in hepatocellular carcinoma and fibrosis following oxygen challenge. J Magn Reson Imaging, 2016, 44(3):37–39.


Článek vyšel v časopise

PLOS One


2019 Číslo 11