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Critical Reviews™ in Biomedical Engineering

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A Review of In Vitro Instrumentation Platforms for Evaluating Thermal Therapies in Experimental Cell Culture Models

Volumen 50, Ausgabe 2, 2022, pp. 39-67
DOI: 10.1615/CritRevBiomedEng.2022043455
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ABSTRAKT

Thermal therapies, the modulation of tissue temperature for therapeutic benefit, are in clinical use as adjuvant or stand-alone therapeutic modalities for a range of indications, and are under investigation for others. During delivery of thermal therapy in the clinic and in experimental settings, monitoring and control of spatio-temporal thermal profiles contributes to an increased likelihood of inducing desired bioeffects. In vitro thermal dosimetry studies have provided a strong basis for characterizing biological responses of cells to heat. To perform an accurate in vitro thermal analysis, a sample needs to be subjected to uniform heating, ideally raised from, and returned to, baseline immediately, for a known heating duration under ideal isothermal condition. This review presents an applications-based overview of in vitro heating instrumentation platforms. A variety of different approaches are surveyed, including external heating sources (i.e., CO2 incubators, circulating water baths, microheaters and microfluidic devices), microwave dielectric heating, lasers or the use of sound waves. We discuss critical heating parameters including temperature ramp rate (heat-up phase period), heating accuracy, complexity, peak temperature, and technical limitations of each heating modality.

Figures

  • Temperature profle of the incubator during heating from 37°C to 42°C steady state with three different runs.
Dot makers show the temperature displayed by the incubator while the solid lines describe actual measured temperature of the sample based on three different runs inside cell culture dish (adapted from Nytko et al.).51
  • (a) Equipment setup for temperature measurement of media in a 96-well plate consisting of fve sealed thermocouples in different wells of the culture plate to monitor the actual sample temperature during hyperthermia exposure. (b) Average measured temperature based on fve temperature probes sealed in different wells of a culture plate at
each time point for different heating techniques (i.e. submerged in water bath, placed in incubator rack with no copper
blocks and with copper blocks) (adapted from Shellman et al.29)
  • Photographic appearance of a water bath system
  • (a) Thermometer set up with two k-type thermocouples placed in a cell carrier-96 plate that was sealed with
an aluminum plate sealer and was heated by immersion in the water bath. (b) measured sample temperature following
floating and submerged cell carrier-96 plate in a preheated water bath at 55°C, shown by blue color (Floating Plate)
and green color (Submerged Plate), respectively (adapted from Massey32).
  • MW radiation system. (a) Experimental set-up including power amplifer and a thermocouple probe connected
to a thermometer for monitoring the temperature during heat exposure. (b) Proposed MW cavity for in vitro heating of
2.75 mL culture medium. (c) Monopole antenna to be enclosed within the MW cavity. (d) Average measured temperature of three samples with standard deviation (SD) error bars (adapted from Kiourti et al.).59
  • Changes in temperature and output of MW irradiation. (a and b) Changes in temperature and output power
within 30 min of MW irradiation (a) and over 0–1min of MW irradiation (b). Sample temperature (shown by blue
color) was monitored by an IR camera and reached the target temperature of 40°C from initial room temperature
within ~ 30 s of MW irradiation, indicating a fast ramp rate (adapted from Asano et al.62)
  • (a) Placement of MW antenna and fber optic sensors during heating experiment where all temperature sensors
were placed within 3 mm spacing from each other with three sensors at the surface and one sensor at the bottom of
the culture well. (b) temperature distribution at four different points during MW heating based on 5 W applied power.
(c) Temperature distribution at four different points during MW heating based on 20 W applied power (adapted from
Manop et al.61)
  • Time-temperature curve based on 15 W MW
heating with three trials (n = 3), indicating a linear relationship between heating time and obtained temperature.
Data are expressed as the mean ± SD among multiple
treatment groups. The times required to reach the target
temperatures of 41, 48 and 60°C were 15, 30 and 60 s,
respectively (adapted from Chen et al.63).
  • Experimental setup for laser irradiation via a dichroic mirror and a perpendicular laser where cells were cultured on glass-bottomed dishes with diagram illustration (a) and photograph (b) of the experimental setup. A diode
laser beam was passed through the dichroic mirror to irradiate a full confluent cultured cell layer perpendicularly on a
glass-based dish. Use of culture medium with no phenol red was reported to avoid blocking diode laser light (adapted
from Inagaki et al.66)
  • Laser light absorption by red blood cells (RBCs) shown in pink color. (a) Without pulsing, laser light absorption rapidly heats the sample (75 µL) to 70°C within 150 s. (b) laser illumination with pulsed on (grey) and pulsed off
(white) to maintain the sample temperature between 36°C and 38°C (adapted from Manderson et al.39)
  • (a) Schematic image of laser irradiation station consisting of a culture dish that was placed on the heating
plate while the cells are placed 12 cm below the laser fber tip for providing identical beam size to the inner diameter
of the dish. (b) Measurement of the temperature distribution at 21 different positions (blue dots) inside the cell culture
dish with fve radial points over four different angles. (c) Non-uniform (bell-shaped) distribution of the measured temperature across the culture dish (reprinted from Miura et al. with permission from JoVE, copyright 201740)
  • The in vitro FUS system. (a) Diagram of experimental design where ultrasound signal was generated using
a piezoelectric focused transducer driven by a signal generator that was immersed at the bottom of a tank flled with
degassed water. (b) and (c) represent measured temperature during FUS exposure that was measured by an IR thermal
camera at 1.142 MHz and 1.467 MHz, respectively. The red, black and blue wavy lines represent the real-time temperatures in three in-parallel sonicated waves (adapted from Zhang et al.76).
  • Temperature distribution during ultrasound exposure throughout the collagen layer. (a and b) Comparison of
simulated (solid line) and measured (markers) maximum temperature and thermal dose shown by black (temperature)
and red (thermal dose), respectively (a) and simulated temperature distributions at different time points ranging from
50 s to 300 s (b) (adapted from Brüningk et al.45)
  • Temperature control during ultrasound heating. (a) Temperature calibration and maintenance at 37°C where
red lines show the approximate rates of the faster ultrasonic and slower chamber heating. (b) Temperature was measured adjacent to the transducer (solid lines) that was dependent on the applied voltage (4−10 V) over the transducer
and within the fluid in the micro-wells (dotted lines) (reprinted from Vanherberghen et al. with permission from The
Royal Society of Chemistry, copyright 201046).
  • Microscale cell culture system. (a) Experimental setup consisting of ITO plate as the main heating component,
a temperature sensor plate made on glass substrate and a cell culture device. (b) Temperature logging designed sensor
layout and temperature sensor plate together with cell culture chamber. Sensor is marked with a green circle while resistors are marked with a red square (reprinted from Mäki et al. with permission from SAGE, copyright 202277).
  • Temperature control. (a) Long-term maintenance of the cell culture temperature with 0.3°C accuracy for
more than 4 days. (b) Measured cell culture temperature during heating experiment where the set-point temperature
was randomly changed, and both Toutside and Tcell were recorded (reprinted from from Mäki et al. with permission from
SAGE, copyright 202277)
  • Temperature control. (a) Photograph of the handheld microcontroller (17.1 cm×11.6 cm×6.5 cm) with an
ITO microheater chip connected and a perfusion block. (b) Temperature profle over time (the set temperature was
37°C and the temperature deviation was evaluated to be within 0.2°C. (c) Two-dimensional IR images of top surface
of ITO microheater chip and chambers. (d) Numerical simulation based temperature evaluation inside the polydimethylsiloxane microbioreactor chamber (reprinted from Nieto et al. with permission from Elsevier, copyright 201779).
  • Experimental setup for IR camera setup used for analyzing the heating capabilities of the microheaters and
an IR image of the microheater including a detailed view of microheater and electrical connectors (a) and an IR image
of the microheater obtained by the thermal camera during heating as well as top view of culture chamber used for performing cell culture (b). The bright spot on the ablation area of the microheater shows the peak temperature of 100°C
(adapted from Nieto et al.83).
  • (a) Schematic of experimental setup for millifluidic release assay. The tube was heated to the desired hyperthermic temperature through a temperature-controlled Peltier element. (b) Fluid entering the capillary tube reached the
desired temperature within 3 mm, corresponding to 0.3 s. The Peltier temperature is measured by a thermocouple and
a control algorithm regulates the output power to control the temperature (reprinted from Burke et al. with permission
from Taylor & Francis, copyright 2018, http://www.tandfonline.com91)
  • (a) Microfluidic chip on the carrier consisting of piezo pumps, cell media reservoirs and the pump connectors and the thermocouple. Each pump is connected to an Eppendorf tube placed vertically inside the carrier
which acts as a cell media reservoir. (b) Temperature distribution measured by IR camera after the recovery of the
cell media turnover inside the microfluidic chip. Figure reproduced from (Catani et al.) under a Creative Commons license.
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