Vitrification and Nanowarming of Kidneys

Anirudh Sharma; Joseph Sushil Rao; Zonghu Han; Lakshya Gangwar; Baterdene Namsrai; Zhe Gao; Hattie L. Ring; Elliott Magnuson; Michael Etheridge; Brian Wowk; Gregory M. Fahy; Michael Garwood; Erik B. Finger; John C. Bischof

doi:10.1002/advs.202101691

Vitrification and Nanowarming of Kidneys

Anirudh Sharma, Joseph Sushil Rao, Zonghu Han, Lakshya Gangwar, Baterdene Namsrai, Zhe Gao, Hattie L. Ring, Elliott Magnuson, Michael Etheridge, Brian Wowk, Gregory M. Fahy, Michael Garwood, Erik B. Finger, John C. Bischof

Research output: Contribution to journal › Article › peer-review

31 Scopus citations

Abstract

Vitrification can dramatically increase the storage of viable biomaterials in the cryogenic state for years. Unfortunately, vitrified systems ≥3 mL like large tissues and organs, cannot currently be rewarmed sufficiently rapidly or uniformly by convective approaches to avoid ice crystallization or cracking failures. A new volumetric rewarming technology entitled “nanowarming” addresses this problem by using radiofrequency excited iron oxide nanoparticles to rewarm vitrified systems rapidly and uniformly. Here, for the first time, successful recovery of a rat kidney from the vitrified state using nanowarming, is shown. First, kidneys are perfused via the renal artery with a cryoprotective cocktail (CPA) and silica-coated iron oxide nanoparticles (sIONPs). After cooling at −40 °C min⁻¹ in a controlled rate freezer, microcomputed tomography (µCT) imaging is used to verify the distribution of the sIONPs and the vitrified state of the kidneys. By applying a radiofrequency field to excite the distributed sIONPs, the vitrified kidneys are nanowarmed at a mean rate of 63.7 °C min⁻¹. Experiments and modeling show the avoidance of both ice crystallization and cracking during these processes. Histology and confocal imaging show that nanowarmed kidneys are dramatically better than convective rewarming controls. This work suggests that kidney nanowarming holds tremendous promise for transplantation.

Original language	English (US)
Article number	2101691
Journal	Advanced Science
Volume	8
Issue number	19
Early online date	Aug 11 2021
DOIs	https://doi.org/10.1002/advs.202101691
State	Published - Oct 2021

Bibliographical note

Funding Information:
The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR-T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi-user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP-OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425-03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046-04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation.

Funding Information:
The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR‐T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi‐user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP‐OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425‐03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046‐04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation.

Publisher Copyright:
© 2021 The Authors. Advanced Science published by Wiley-VCH GmbH

Keywords

cryopreservation
iron oxide nanoparticles
kidney
perfusion
radiofrequency warming
vitrification

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural

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10.1002/advs.202101691

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@article{171e6b1f6d9a40958942b33482246170,

title = "Vitrification and Nanowarming of Kidneys",

abstract = "Vitrification can dramatically increase the storage of viable biomaterials in the cryogenic state for years. Unfortunately, vitrified systems ≥3 mL like large tissues and organs, cannot currently be rewarmed sufficiently rapidly or uniformly by convective approaches to avoid ice crystallization or cracking failures. A new volumetric rewarming technology entitled “nanowarming” addresses this problem by using radiofrequency excited iron oxide nanoparticles to rewarm vitrified systems rapidly and uniformly. Here, for the first time, successful recovery of a rat kidney from the vitrified state using nanowarming, is shown. First, kidneys are perfused via the renal artery with a cryoprotective cocktail (CPA) and silica-coated iron oxide nanoparticles (sIONPs). After cooling at −40 °C min−1 in a controlled rate freezer, microcomputed tomography (µCT) imaging is used to verify the distribution of the sIONPs and the vitrified state of the kidneys. By applying a radiofrequency field to excite the distributed sIONPs, the vitrified kidneys are nanowarmed at a mean rate of 63.7 °C min−1. Experiments and modeling show the avoidance of both ice crystallization and cracking during these processes. Histology and confocal imaging show that nanowarmed kidneys are dramatically better than convective rewarming controls. This work suggests that kidney nanowarming holds tremendous promise for transplantation.",

keywords = "cryopreservation, iron oxide nanoparticles, kidney, perfusion, radiofrequency warming, vitrification",

author = "Anirudh Sharma and Rao, {Joseph Sushil} and Zonghu Han and Lakshya Gangwar and Baterdene Namsrai and Zhe Gao and Ring, {Hattie L.} and Elliott Magnuson and Michael Etheridge and Brian Wowk and Fahy, {Gregory M.} and Michael Garwood and Finger, {Erik B.} and Bischof, {John C.}",

note = "Funding Information: The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR-T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi-user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP-OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425-03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046-04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation. Funding Information: The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR‐T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi‐user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP‐OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425‐03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046‐04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation. Publisher Copyright: {\textcopyright} 2021 The Authors. Advanced Science published by Wiley-VCH GmbH",

year = "2021",

month = oct,

doi = "10.1002/advs.202101691",

language = "English (US)",

volume = "8",

journal = "Advanced Science",

issn = "2198-3844",

publisher = "Wiley-VCH Verlag",

number = "19",

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TY - JOUR

T1 - Vitrification and Nanowarming of Kidneys

AU - Sharma, Anirudh

AU - Rao, Joseph Sushil

AU - Han, Zonghu

AU - Gangwar, Lakshya

AU - Namsrai, Baterdene

AU - Gao, Zhe

AU - Ring, Hattie L.

AU - Magnuson, Elliott

AU - Etheridge, Michael

AU - Wowk, Brian

AU - Fahy, Gregory M.

AU - Garwood, Michael

AU - Finger, Erik B.

AU - Bischof, John C.

N1 - Funding Information: The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR-T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi-user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP-OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425-03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046-04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation. Funding Information: The authors thank the Center for Magnetic Resonance and Research's (CMRR UMN) Dr. D. Idiyatullin for MR‐T1 scans on samples, S. Ramesh for processing tissue slices for analysis, C. Forster and A. Lewis from the Clinical and Translational Science Institute (CTSI UMN) for technical assistance with histology and imaging; M. Lotti for assistance with writing; Dr. N. Manuchehrabadi for help with supplementary rabbit nanowarming data. J.S.R. was supported by Schulze Diabetes Institute and Division of Transplantation at the Department of Surgery, University of Minnesota. The authors acknowledge Schulze Diabetes Institute, Department of Surgery for their confocal microscope. The authors would like to thank Dr. D. Bilardello at the Institute of Rock Magnetism (IRM) for his guidance in magnetic measurements. Part of this work was performed at the Institute for Rock Magnetism (IRM) at the University of Minnesota. The IRM is a US National Multi‐user Facility supported through the Instrumentation and Facilities program of the National Science Foundation, Earth Sciences Division, and by funding from the University of Minnesota. The authors thank Y. Liu for her assistance with DLS measurements of sIONPs. The authors also thank the University Imaging Center (UIC) and Research Analytical laboratory (RAL) at UMN for technical assistance in imaging and ICP‐OES measurements. This work was supported by the National Institutes of Health Grant 5R01DK117425‐03 (J.C.B., E.B.F.), National Institute of Health Grant 5R01HL135046‐04 (J.C.B., E.B.F.), and National Science Foundation Grant EEC 1941543 (J.C.B., E.B.F.). The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official NIH or NSF position, policy, or decision unless so designated by other documentation. Publisher Copyright: © 2021 The Authors. Advanced Science published by Wiley-VCH GmbH

PY - 2021/10

Y1 - 2021/10

N2 - Vitrification can dramatically increase the storage of viable biomaterials in the cryogenic state for years. Unfortunately, vitrified systems ≥3 mL like large tissues and organs, cannot currently be rewarmed sufficiently rapidly or uniformly by convective approaches to avoid ice crystallization or cracking failures. A new volumetric rewarming technology entitled “nanowarming” addresses this problem by using radiofrequency excited iron oxide nanoparticles to rewarm vitrified systems rapidly and uniformly. Here, for the first time, successful recovery of a rat kidney from the vitrified state using nanowarming, is shown. First, kidneys are perfused via the renal artery with a cryoprotective cocktail (CPA) and silica-coated iron oxide nanoparticles (sIONPs). After cooling at −40 °C min−1 in a controlled rate freezer, microcomputed tomography (µCT) imaging is used to verify the distribution of the sIONPs and the vitrified state of the kidneys. By applying a radiofrequency field to excite the distributed sIONPs, the vitrified kidneys are nanowarmed at a mean rate of 63.7 °C min−1. Experiments and modeling show the avoidance of both ice crystallization and cracking during these processes. Histology and confocal imaging show that nanowarmed kidneys are dramatically better than convective rewarming controls. This work suggests that kidney nanowarming holds tremendous promise for transplantation.

AB - Vitrification can dramatically increase the storage of viable biomaterials in the cryogenic state for years. Unfortunately, vitrified systems ≥3 mL like large tissues and organs, cannot currently be rewarmed sufficiently rapidly or uniformly by convective approaches to avoid ice crystallization or cracking failures. A new volumetric rewarming technology entitled “nanowarming” addresses this problem by using radiofrequency excited iron oxide nanoparticles to rewarm vitrified systems rapidly and uniformly. Here, for the first time, successful recovery of a rat kidney from the vitrified state using nanowarming, is shown. First, kidneys are perfused via the renal artery with a cryoprotective cocktail (CPA) and silica-coated iron oxide nanoparticles (sIONPs). After cooling at −40 °C min−1 in a controlled rate freezer, microcomputed tomography (µCT) imaging is used to verify the distribution of the sIONPs and the vitrified state of the kidneys. By applying a radiofrequency field to excite the distributed sIONPs, the vitrified kidneys are nanowarmed at a mean rate of 63.7 °C min−1. Experiments and modeling show the avoidance of both ice crystallization and cracking during these processes. Histology and confocal imaging show that nanowarmed kidneys are dramatically better than convective rewarming controls. This work suggests that kidney nanowarming holds tremendous promise for transplantation.

KW - cryopreservation

KW - iron oxide nanoparticles

KW - kidney

KW - perfusion

KW - radiofrequency warming

KW - vitrification

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U2 - 10.1002/advs.202101691

DO - 10.1002/advs.202101691

M3 - Article

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AN - SCOPUS:85112340709

SN - 2198-3844

VL - 8

JO - Advanced Science

JF - Advanced Science

IS - 19

M1 - 2101691

ER -

Vitrification and Nanowarming of Kidneys

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

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ATP-Bio: NSF Engineering Research Center for Advanced Technologies for the Preservation of Biological Systems (ATP-Bio)

Organ banking for transplant-kidney cryopreservation by

Breakthrough Tissue and Organ Preservation and Transplan

Huron TissueScope LE

Slide Scanning

University Imaging Centers

Cite this

Vitrification and Nanowarming of Kidneys

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

Publisher link

Find It

Other files and links

Fingerprint

Projects

ATP-Bio: NSF Engineering Research Center for Advanced Technologies for the Preservation of Biological Systems (ATP-Bio)

Organ banking for transplant-kidney cryopreservation by

Breakthrough Tissue and Organ Preservation and Transplan

University Assets

Huron TissueScope LE

Slide Scanning

University Imaging Centers

Cite this