Zonghu Han’s research while affiliated with University of Minnesota, Duluth and other places

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Publications (40)


A rapid and scalable rewarming platform technique using joule heating
a Schematics of biological systems cryopreservation using plunge cooling and joule heating. The biological systems loaded with cryoprotective agent (CPA) were in contact with the electrical conductor. After removing the excess CPA solution, the biological systems and electrical conductor were plunged together into liquid nitrogen (LN2) for cooling. For rewarming, the electrical conductor was connected to a voltage pulse generator and generated heat via joule heating. The biomaterial was rewarmed via conduction. Drawings not to scale. b Three types of biosystems with different thicknesses were used as the model systems, including adherent cells (4 µm), Drosophila embryos (50 µm), and kidney slices (1.2 mm), as shown in the plot (drawings not to scale). The heat diffusion time (td, right y-axis) across the biosystems is positively correlated with the biosystem thickness.
Characterization of joule heating using a pulse generator
a The R-C discharge circuit is used to generate joule heating by connecting the electrical conductor to a pulse generator. The voltage and pulse width can be adjusted. The capacitance (C) is 4000 µF. Ranges of the current (I), voltage (V), and pulse width (pw) for the low voltage mode (LV, ≤ 500 V) are listed in the figure. b Stainless steel (SS) sheet and mesh were used in this study. The thickness of SS sheet is 12 µm. The wire diameter and aperture size of the SS mesh are 30 and 38 µm, respectively. The SS mesh allows easy removal of excess CPA solution. c The electrical conductivity (σ) of the SS sheet and mesh can be calculated from the resistance by measuring the voltage and current. n = 6 independent experiments. d Comparison of various materials for rapid warming rate. The warming rate is inversely correlated to material density (ρ), electrical conductivity (σ), and heat capacity (Cp). Details in Eq. 7 assuming same electrical current, material dimensions and pulse width. e Voltage profile when different voltage pulse widths were used. The exponential decay of measured voltage matched with the calculated voltage of a R-C discharge circuit. f Voltage profile when multiple voltage pulses were applied. g Maximum energy delivered per pulse depends on the resistance and pulse width. For R ≤ 1 Ω, the max current of 500 A is used for calculation. For R ≥ 1 Ω, the max voltage of 500 V is used for calculation. h Temperature profile of a thin film resistor (150 Ω) when subjected to a voltage pulse of 300 V, 5 ms. A thermocouple was attached to the electrically insulated surface of the resistor. The resistor was submerged in liquid nitrogen (LN2) during the measurement. Sampling resolution was 1 ms. i Temperature change (ΔT) as a function of applied voltage. The same setup shown in h was used. n = 6 independent experiments. For c and i, data presented as mean ± s.d.
Adherent cells cryopreservation using joule heating
a Simulated temperature profile of stainless steel (SS) sheet and cell monolayer under pulse width (pw) ranging from 1 µs to 1 ms (shared y axis). The warming rates at the middle of SS sheet (point A), middle of cells (point B), and top of cells (point C) are displayed. b Simulated temperature (in black) and measured viability (in red) of human dermal fibroblasts (HDFs) for 1 ms and 100 µs pulse width with different voltages. VS55 (i.e., 55 wt%) was used as the cryoprotective agent (CPA). n = 4 independent experiments. Data presented as mean ± s.d. c Merged Hoechst/Propidium Iodide (PI) images of HDF cells. Conditions including underheating, good warming, overheating (for joule heating, as numbered in b), and positive control are shown. The pulse width is 1 ms. Scale bar is 500 µm. d Estimated critical warming rate (CWR) plotted as a function of CPA concentration. Propylene glycol (PG, good glass-forming tendency) and glycerol (poor glass-forming tendency) were used to estimate the range of CWR (orange area) of different CPA concentrations. In this study, 13.75%, 27.5%, 41.25%, and 55% CPA were tested. The measured convective warming rate (WR) were marked in the plot, along with the simulated WR of 1 ms, 100 µs, and 10 µs pulse joule heating. The experimentally tested conditions were labelled as dots at the intersections of CPA concentrations and warming rates. e Post-thaw viability of HDF cells using different CPA concentrations and warming methods. Vitrification failure (i.e., ice formation) was noted for 13.27% and 27% CPA groups. n = 4 independent experiment. Bounds and horizontal line of box represent standard deviation and mean, respectively; whiskers represent max and min. f For 13.75% CPA, merged Hoechst/PI images of HDF cells rewarmed by convective warming, 1 ms, 100 µs, and 10 µs pulse joule heating. Scale bar is 500 µm. One-way ANOVA and Tukey’s post hoc were used for statistical analysis. ns, p > 0.05.
Drosophila embryos cryopreservation using joule heating
a Images of the Drosophila embryos on the stainless steel (SS) mesh after cooling. Embryos were loaded with different ethylene glycol (EG) concentrations. b Geometry and dimensions of the SS mesh and embryos used in the heat transfer modeling. Points A, B, and C represent the top, middle and bottom of the embryo, respectively. Point D and E represent the SS mesh in contact with the embryo and outside the embryo, respectively. c Temperature profile at different locations for 1 ms joule heating. d Warming rate distribution at the middle plane of embryos. e Warming rate of the embryo for different joule heating pulse widths. f Images of embryos on the SS mesh acquired by a high-speed camera at 3000 fps. The cryoprotective agent (CPA) was 27% EG + 9% sorbitol. The voltage was 290 V. g Normalized grayscale intensity of the embryos was plotted from the high-speed camera videos. Ice (i.e., white color) showed a high intensity value. Different CPA concentrations (labelled as EG + sorbitol concentration) were tested. n = 5. Data presented as mean ± s.d. h Survival of embryos after exposure to different CPA concentrations. Hatch and adult rates represent the survival from embryos to larvae and larvae to adults, respectively. n = 4. i Temperature of the embryos after 1 ms joule heating using different voltages. j Survival of embryos after 1 ms joule heating using different voltages. The CPA was 27% EG + 9% sorbitol. n = 8. k Comparison of embryo survival using convective warming and joule heating (290 V, 1 ms) for different CPA concentrations. n = 8. For a and f, scale bar is 500 µm. For g–j, n represent independent experiments. For h, j, and k, bounds and horizontal line of box represent standard deviation and mean respectively; whiskers represent max and min. For c–e, i modeling results were shown. Multivariate analysis of variance (MANOVA) and Tukey’s post hoc were used for statistical analysis. ns, p > 0.05.
Kidney slice cryopreservation using joule heating
a Rat kidney slices of 1.2 mm thickness and 6 mm in diameter were used. After cryoprotective agent (CPA) loading, the kidney slice was sandwiched using the stainless steel (SS) mesh prior to plunge-cooling in liquid nitrogen, then rewarmed by connecting the SS mesh to a voltage source. b Warming rate distribution within the kidney slice. Point A represents the SS mesh; B, C, and D represent the kidney slice. The detailed locations of points A, B, C, and D were marked in the plot. c Temperature profile at different locations (point A to D) for 100 ms joule heating. d Warming rates at different locations within the kidney slice using 10 ms, 100 ms, and 1000 ms joule heating. e CPA concentration distribution within the kidney slice after loading with different CPA concentrations. f Viability of kidney slices after exposure to different CPA concentrations. n = 9 independent samples. g Post-thaw viability of the kidney slices by joule heating using different voltages. The CPA is 50% VS55. n = 8 independent samples. h Comparison of post-thaw viability of kidney slices using convective warming and joule heating for different CPA concentrations. n = 8 independent samples. i Histology (H & E staining) of kidney slices. Arrowhead showed disrupted glomeruli, and arrow indicated damaged proximal tubules. Scale bar is 500 µm. Modeling results were shown in b–e. For f–h, the viability was measured by alamarBlue assay and normalized by the readings prior to treatment. Date presented as mean ± s.d. One-way ANOVA and Tukey’s post hoc were used for statistical analysis.

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Rapid joule heating improves vitrification based cryopreservation
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October 2022

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448 Reads

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30 Citations

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Zonghu Han

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Cryopreservation by vitrification has far-reaching implications. However, rewarming techniques that are rapid and scalable (both in throughput and biosystem size) for low concentrations of cryoprotective agent (CPA) for reduced toxicity are lacking, limiting the potential for translation. Here, we introduce a joule heating–based platform technology, whereby biosystems are rapidly rewarmed by contact with an electrical conductor that is fed a voltage pulse. We demonstrate successful cryopreservation of three model biosystems with thicknesses across three orders of magnitude, including adherent cells (~4 µm), Drosophila melanogaster embryos (~50 µm) and rat kidney slices (~1.2 mm) using low CPA concentrations (2–4 M). Using tunable voltage pulse widths from 10 µs to 100 ms, numerical simulation predicts that warming rates from 5 × 10⁴ to 6 × 10⁸ °C/min can be achieved. Altogether, our results present a general solution to the cryopreservation of a broad spectrum of cellular, organismal and tissue-based biosystems.

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Cryopreservation of Whole Rat Livers by Vitrification and Nanowarming

October 2022

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126 Reads

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32 Citations

Annals of Biomedical Engineering

Liver cryopreservation has the potential to enable indefinite organ banking. This study investigated vitrification—the ice-free cryopreservation of livers in a glass-like state—as a promising alternative to conventional cryopreservation, which uniformly fails due to damage from ice formation or cracking. Our unique “nanowarming” technology, which involves perfusing biospecimens with cryoprotective agents (CPAs) and silica-coated iron oxide nanoparticles (sIONPs) and then, after vitrification, exciting the nanoparticles via radiofrequency waves, enables rewarming of vitrified specimens fast enough to avoid ice formation and uniformly enough to prevent cracking from thermal stresses, thereby addressing the two main failures of conventional cryopreservation. This study demonstrates the ability to load rat livers with both CPA and sIONPs by vascular perfusion, cool them rapidly to an ice-free vitrified state, and rapidly and homogenously rewarm them. While there was some elevation of liver enzymes (Alanine Aminotransferase) and impaired indocyanine green (ICG) excretion, the nanowarmed livers were viable, maintained normal tissue architecture, had preserved vascular endothelium, and demonstrated hepatocyte and organ-level function, including production of bile and hepatocyte uptake of ICG during normothermic reperfusion. These findings suggest that cryopreservation of whole livers via vitrification and nanowarming has the potential to achieve organ banking for transplant and other biomedical applications.


Injectable and Repeatable Inductive Heating of Iron Oxide Nanoparticle-Enhanced "PHIL" Embolic toward Tumor Treatment

September 2022

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35 Reads

ACS Applied Materials & Interfaces

Deep-seated tumors of the liver, brain, and other organ systems often recur after initial surgical, chemotherapeutic, radiation, or focal treatments. Repeating these treatments is often invasive and traumatic. We propose an iron oxide nanoparticle (IONP)-enhanced precipitating hydrophobic injectable liquid (PHIL, MicroVention inc.) embolic as a localized dual treatment implant for nutrient deprivation and multiple repeatable thermal ablation. Following a single injection, multiple thermal treatments can be repeated as needed, based on monitoring of tumor growth/recurrence. Herein we show the ability to create an injectable stable PHIL-IONP solution, monitor deposition of the PHIL-IONP precipitate dispersion by μCT, and gauge the IONP distribution within the embolic by magnetic resonance imaging. Once precipitated, the implant could be heated to reach therapeutic temperatures >8 °C for thermal ablation (clinical temperature of ∼45 °C), in a model disk and a 3D tumor bed model. Heat output was not affected by physiological conditions, multiple heating sessions, or heating at intervals over a 1 month duration. Further, in ex vivo mice hind-limb tumors, we could noninvasively heat the embolic to an "ablative" temperature elevation of 17 °C (clinically 54 °C) in the first 5 min and maintain the temperature rise over +8 °C (clinically a temperature of 45 °C) for longer than 15 min.


Pancreatic islet cryopreservation by vitrification achieves high viability, function, recovery and clinical scalability for transplantation

April 2022

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395 Reads

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69 Citations

Nature Medicine

Pancreatic islet transplantation can cure diabetes but requires accessible, high-quality islets in sufficient quantities. Cryopreservation could solve islet supply chain challenges by enabling quality-controlled banking and pooling of donor islets. Unfortunately, cryopreservation has not succeeded in this objective, as it must simultaneously provide high recovery, viability, function and scalability. Here, we achieve this goal in mouse, porcine, human and human stem cell (SC)-derived beta cell (SC-beta) islets by comprehensive optimization of cryoprotectant agent (CPA) composition, CPA loading and unloading conditions and methods for vitrification and rewarming (VR). Post-VR islet viability, relative to control, was 90.5% for mouse, 92.1% for SC-beta, 87.2% for porcine and 87.4% for human islets, and it remained unchanged for at least 9 months of cryogenic storage. VR islets had normal macroscopic, microscopic, and ultrastructural morphology. Mitochondrial membrane potential and adenosine triphosphate (ATP) levels were slightly reduced, but all other measures of cellular respiration, including oxygen consumption rate (OCR) to produce ATP, were unchanged. VR islets had normal glucose-stimulated insulin secretion (GSIS) function in vitro and in vivo. Porcine and SC-beta islets made insulin in xenotransplant models, and mouse islets tested in a marginal mass syngeneic transplant model cured diabetes in 92% of recipients within 24–48 h after transplant. Excellent glycemic control was seen for 150 days. Finally, our approach processed 2,500 islets with >95% islets recovery at >89% post-thaw viability and can readily be scaled up for higher throughput. These results suggest that cryopreservation can now be used to supply needed islets for improved transplantation outcomes that cure diabetes.




Vitrification and Rewarming of Magnetic Nanoparticle‐Loaded Rat Hearts

October 2021

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215 Reads

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45 Citations

To extend the preservation of donor hearts beyond the current 4–6 h, this paper explores heart cryopreservation by vitrification—cryogenic storage in a glass‐like state. While organ vitrification is made possible by using cryoprotective agents (CPA) that inhibit ice during cooling, failure occurs during convective rewarming due to slow and non‐uniform rewarming which causes ice crystallization and/or cracking. Here an alternative, “nanowarming”, which uses silica‐coated iron oxide nanoparticles (sIONPs) perfusion loaded through the vasculature is explored, that allows a radiofrequency coil to rewarm the organ quickly and uniformly to avoid convective failures. Nanowarming has been applied to cells and tissues, and a proof of principle study suggests it is possible in the heart, but proper physical and biological characterization especially in organs is still lacking. Here, using a rat heart model, controlled machine perfusion loading and unloading of CPA and sIONPs, cooling to a vitrified state, and fast and uniform nanowarming without crystallization or cracking is demonstrated. Further, nanowarmed hearts maintain histologic appearance and endothelial integrity superior to convective rewarming and indistinguishable from CPA load/unload control hearts while showing some promising organ‐level (electrical) functional activity. This work demonstrates physically successful heart vitrification and nanowarming and that biological outcomes can be expected to improve by reducing or eliminating CPA toxicity during loading and unloading.



Vitrification and Nanowarming of Kidneys

August 2021

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535 Reads

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62 Citations

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.


Averaged extinction cross-section of aggregated 5, 16, and 30 nm GNP by spectra plots (a) and contour plots produced with fitting and smoothing algorithms (b). (a) Number on the left of the y-axis indicate the number of GNPs in the aggregate. A second peak can be observed for 2 particle aggregations at various wavelength and gradually diminished with increase of aggregation sizes up to 30 (5 and 16 nm GNP) and up to 20 (30 nm GNP).
(a) Plasmon resonance peak of aggregated GNP. The larger the aggregation size and the larger the GNP diameter, the more red shifted the aggregated cluster will be. (b) Averaged per-particle extinction cross-section plots of 5, 16, and 30 nm diameter GNP aggregations at the resonance peak (532 nm (green laser heating) and 808 nm (NIR laser heating)). (c) To explore the way to generate the most heat by the same amount of gold, the extinction coefficient (Qext) of 1, 3, and 20 particle clusters with very close effective radius (< 1% difference) are compared. We can see the single GNP has the highest extinction at resonance peak, while an aggregation cluster with larger number of GNP is slightly better than the small cluster.
GNP aggregation photothermal conversion experiment preparation. (a) Experiment scheme: induce and fix controlled-size GNP aggregation in solution and test by cuvette settings. (b) Visual picture, DLS and UV–Vis characterization of GNP aggregation solutions. (c) TEM Characterization of GNP aggregation solution samples in (b), 100 nm scale bar.
(a) Photothermal conversion experiment result of aggregated GNPs under 190 mW 532 nm wavelength CW laser. Large aggerates formed by 16 nm and 30 nm GNP showed significant lower heat comparing to discrete GNPs *p < 0.05, **p < 0.01. (b) Heat generation by converting optical properties predicted in modelling. Heating is shown to decline consistently with larger size aggregates. Predicted heat pointed by red arrows correspond to experimental heat generated by GNS aggregate with 400 mM NaCl addition.
Aggregation affects optical properties and photothermal heating of gold nanospheres

January 2021

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438 Reads

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28 Citations

Laser heating of gold nanospheres (GNS) is increasingly prevalent in biomedical applications due to tunable optical properties that determine heating efficiency. Although many geometric parameters (i.e. size, morphology) can affect optical properties of individual GNS and their heating, no specific studies of how GNS aggregation affects heating have been carried out. We posit here that aggregation, which can occur within some biological systems, will significantly impact the optical and therefore heating properties of GNS. To address this, we employed discrete dipole approximation (DDA) simulations, Ultraviolet–Visible spectroscopy (UV–Vis) and laser calorimetry on GNS primary particles with diameters (5, 16, 30 nm) and their aggregates that contain 2 to 30 GNS particles. DDA shows that aggregation can reduce the extinction cross-section on a per particle basis by 17–28%. Experimental measurement by UV–Vis and laser calorimetry on aggregates also show up to a 25% reduction in extinction coefficient and significantly lower heating (~ 10%) compared to dispersed GNS. In addition, comparison of select aggregates shows even larger extinction cross section drops in sparse vs. dense aggregates. This work shows that GNS aggregation can change optical properties and reduce heating and provides a new framework for exploring this effect during laser heating of nanomaterial solutions.


Citations (18)


... 101 Several studies have demonstrated that the colloidal and thermal stability of MNPs in VS55 can be maintained though surface coating with resorcinol-formaldehyde resin or silica. [104][105][106][107] Additionally, surface modification with poly(ethylene glycol) has been shown to reduce cellular interactions and thus cytotoxicity. 106,107 Manuchehrabadi achieved nanowarming of porcine arteries and porcine aortic heart valve leaflet tissues using magnetic heating. ...

Reference:

Advances in magnetic nanoparticles for molecular medicine
Magnetic-Nanorod-Mediated Nanowarming with Uniform and Rate-Regulated Heating
  • Citing Article
  • September 2024

Nano Letters

... 101 Several studies have demonstrated that the colloidal and thermal stability of MNPs in VS55 can be maintained though surface coating with resorcinol-formaldehyde resin or silica. [104][105][106][107] Additionally, surface modification with poly(ethylene glycol) has been shown to reduce cellular interactions and thus cytotoxicity. 106,107 Manuchehrabadi achieved nanowarming of porcine arteries and porcine aortic heart valve leaflet tissues using magnetic heating. ...

Engineering Magnetic Nanoclusters for Highly Efficient Heating in Radio-Frequency Nanowarming
  • Citing Article
  • April 2024

Nano Letters

... Researchers have effectively used different combinations of these CPAs, particularly EG and DMSO, on a variety of tissues and cells, including amnion-derived MSCs [39], cord blood [40], and embryos [41]. High concentrations of CPAs are necessary for the equilibrium vitrification process, which can potentially be detrimental to cells [42]. Consequently, the vitrification freezing method often requires both careful preparation of the CPA mixture and the gradual injection of the CPA at lower temperatures to ensure maximum safety. ...

Model-guided design and optimization of CPA perfusion protocols for whole organ cryopreservation
  • Citing Article
  • December 2023

Cryobiology

... Hence, the minimum CPA concentration for vitrification would be ~62% w/w, which is slightly lower than M22 (~66%w/w which includes carrier solution), where we have shown successful vitrification at 3L. Higher concentrations of CPAs such as VS83 (83% w/w CPA) have even lower CCR and can be more easily vitrified but increase biological toxicity relative to the CPAs chosen here [34]. To remain at a lower concentration of CPA and still achieve vitrification at higher volumes without toxicity, future work can assess the impact of ice recrystallization inhibitors (IRIs), polymers (e.g., polyglycerol-PGL, polyvinyl alcohol-PVA, polyethylene glycol-PEG, x-1000, z-1000, etc.), or other novel cryoprotective agents [35,36]. ...

Model-Guided Design and Optimization of CPA Perfusion Protocols for Whole Organ Cryopreservation

Annals of Biomedical Engineering

... Specimens have to be stored below −130 °C to avoid devitrification. Functional cryopreservation by vitrification is an active field of basic research, and has been successfully applied to the rat kidney and liver [31,32]. Functional cryopreservation has not yet been demonstrated for the whole adult mammalian brain, let alone body [33][34][35][36][37][38][39][40]. ...

Vitrification and nanowarming enable long-term organ cryopreservation and life-sustaining kidney transplantation in a rat model

... Therefore warming rate is an important consideration in combatting freezing damage (Gao and Critser, 2000;Waters et al., 2020). In particular, a sample that has undergone vitrification may be especially susceptible to ice recrystallization if the warming rate is too slow (Bojic et al., 2021;Zhan et al., 2022). ...

Rapid joule heating improves vitrification based cryopreservation
  • Citing Article
  • December 2022

Cryobiology

... Apoptosis results when electrical pulses that are administered to cancer cells provoke thermal damage to internal structures and cell membranes [4]; it is known as inhibition of Fractal Fract. 2025, 9,34 2 of 20 proliferation on biological cells [5]. Healthy cells that are in the surrounding media are less sensitive to applied electrical pulses, avoiding significant damage. ...

Rapid joule heating improves vitrification based cryopreservation

... Specimens have to be stored below −130 °C to avoid devitrification. Functional cryopreservation by vitrification is an active field of basic research, and has been successfully applied to the rat kidney and liver [31,32]. Functional cryopreservation has not yet been demonstrated for the whole adult mammalian brain, let alone body [33][34][35][36][37][38][39][40]. ...

Cryopreservation of Whole Rat Livers by Vitrification and Nanowarming
  • Citing Article
  • October 2022

Annals of Biomedical Engineering

... Islets of Langerhans are mini-organs, cryopreserved islets or islets that have been cultured for a longer period, are usually not suitable for islet transplantation 2,4-8 . Although a great progress has been made in the cryopreservation of human islets 8 , in vitro culture of human islets, which will subject islets to stress, is still a necessary and critical step in islet transplantation, so that the quality and quantity of donor islets can be evaluated, and it also provides additional time to get recipients ready for the operation. In vitro culture of islets will also allow researchers to study their function, to characterize the subtype of cells in human islets, and to study the function of pancreatic genes or subtypes of cells. ...

Pancreatic islet cryopreservation by vitrification achieves high viability, function, recovery and clinical scalability for transplantation

Nature Medicine

... In recent years, studies on organ and tissue cryopreservation have highlighted the importance of proper cryoprotectant addition. Contemporary cryoprotectants, like M22, VMP and VS55, contain any combination of the most commonly used cryoprotecting agents, ethylene glycol (EG) and DMSO [27], which have been used extensively in cryoprotection of human oocytes and zygotes [28], ovarian tissue [29], rat and rabbit kidneys [30,31], mouse hearts [32], and lamb cartilage [33]. ...

Vitrification and Rewarming of Magnetic Nanoparticle-Loaded Rat Hearts
  • Citing Article
  • December 2021

Cryobiology