Research ArticleExperimental Studies
Open Access

Physical Properties of Ultrafine Bubbles Generated Using a Generator System

SHINGO MIYAMOTO, TOYOFUMI HIRAKAWA, YUKIKO NOGUCHI, DAICHI URUSHIYAMA, KOHEI MIYATA, TSUKASA BABA, FUSANORI YOTSUMOTO, SHIN’ICHIRO YASUNAGA, KAZUHIKO NAKABAYASHI, KENICHIRO HATA, WATARU NAKAGAWA, TOSHIHIRO OTSUKA, YOSHIKO NOZAWA, IPPEI FURUHATA and JITSUO MIKASA
In Vivo November 2023, 37 (6) 2555-2563; DOI: https://doi.org/10.21873/invivo.13363

Abstract

Background/Aim: Ultrafine bubbles (UFBs) have been extensively researched owing to their promising physical and biological properties. However, determining the lifespan or ideal concentration of UFBs for various biological events is challenging. This study aimed to determine the maximum concentration and longest lifespan of UFBs and to verify the validity of UFBs for assessing cell properties. Materials and Methods: A generator system (HMB-H0150+P001, TOSSLEC Corporation Limited, Kyoto, Japan) generated UFBs using various gases. The size and concentration of UFBs in ultrapure water and cell culture medium were measured through a nanoparticle tracking analysis method. Results: The UFB concentration increased when the generator operated in a time dependent manner. The mean size of UFBs was approximately 120 nm. In the UFB lifespan, the concentration decreased by approximately 30% within the first two weeks of generation and was stable for up to 6 months. The UFB size increased by approximately 20% within the first two weeks of generation and demonstrated minor changes until the 6th month. The number of cells differed significantly with various concentrations of nitrogen gas UFBs. Conclusion: The generator system can generate UFBs with multiple concentrations within a suitable temperature. Consequently, the solution containing UFBs could be widely acceptable in cell culture systems.

Key Words:

Ultrafine bubbles (UFBs) or bulk nanobubbles (NBs), are gas-filled cavities with sizes less than 1000 nm in liquid. According to typical thermodynamics, the majority of the UFBs diffuse and vanish in water within less than a few seconds owing to high internal pressures (1, 2). In recent years, several studies have reported promising data stating that UFBs can retain their form in water for long periods (3, 4). Some unique properties of UFBs are that they possess an extremely specific surface area in liquid, considering their small size, and the amount of UFBs can be markedly elevated due to the stability of UFBs in the presence of periodic pressure change unlike micro or macro-sized bubbles (5). Michailidi et al. described that the hydrogen bonding interactions primarily contribute to the long-time stability of generated bulk nanobubbles, which is up to three months (6). Owing to these unique physicochemical properties, UFBs have gained popularity in various areas (7-10), including biomedical applications (11, 12). However, research on the advantages and disadvantages of UFBs in scientific applications is limited.

Recently, extensive research on the biological effects of UFBs and nanomaterials on diverse creatures has been conducted (6, 13-19). The effects of UFBs on plant, fish, and animal growth were evaluated. The results indicated that UFBs promoted the growth and weight gain of fish, plants, and animals (10). However, the mechanism of UFBs in growth advancement remains unclear. The biological effects of UFBs were evaluated by comparing seed germination in UFB-filled water with that in distilled water without UFBs, indicating that UFBs triggered seed germination in contrast to distilled water. The four types of reactive oxygen stress (ROS) including superoxide anion radical (O2·−), hydrogen peroxide (H2O2), hydroxyl radical (·OH), and singlet oxygen (1O2) were measured using a fluorescent reagent APF, Fenton reaction, dismutation reaction of superoxide dismutase, and DMSO. Further, ·OH was confirmed to be the specific ROS produced with nanobubbles by water (15). The levels of superoxide radicals in UFB-filled water were similar to those in a 0.3 mM H2O2 solution, which were more substantially elevated than those in distilled water. The reactive oxygen species involved in UFBs were believed to be associated with seed germination. In addition, UFBs adsorbed on the surface of polystyrene films were used as a cell culture scaffold for mouse fibroblast L929 cells, indicating that UFBs can induce fibroblast cell proliferation (20). The results indicated a positive effect of UFBs on cells, plants, and animals. In contrast, the same study also revealed that the suppressive/negative effects of UFBs were found in a cell culture with a human leukemia cell line (HL60), suggesting that the UFB properties may differ between adherent and non-adherent cells (20). Owing to the unpredictability of UFBs, elucidating their mechanism by investigating each case in detail is necessary. The potential of nitrogen gas nanobubbles in fibroblast proliferation was investigated, suggesting that nitrogen gas nanobubbles in the culture medium may promote cell proliferation (21). In a culture medium comprising air and oxygen UFBs, the high-oxygen-content UFBs significantly inhibited the dental follicle stem cell proliferation compared with the low-oxygen-content UFBs (22). Based on the above studies, the effects of UFBs on bioactivation may differ slightly according to the type of organism or kind of gas in the UFBs. Notably, only a few studies based on cell proliferation used a cell medium containing UFBs (20-22).

Various stimulating factors, including cytokines, growth factors, hormones, electrical signals, and mechanical forces, control cell growth (23). Proliferation is a living cell property influenced by external stimulation. Thus, cell proliferation can be observed and analyzed easily and quickly. Enhancing cell proliferation is significant to tissue engineering and regenerative medicine. Various stimuli, including biological factors and engineered conditions, have been investigated to improve cell proliferation. Hypoxic conditions and fibroblast growth factor-2 improved human bone marrow stromal cell proliferation (24). Regarding cell division, the mouse fibroblast cell line L929 responded positively to electric stimulation (25). Recently, UFBs have been explored for their applicability for cell proliferation enhancement. However, research on the adverse effects of UFBs on cells for long cell culture periods is limited.

Previous research has shown that UFBs have a promising potential for biological applications. However, the adequate concentration of UFBs for cell culture and the duration for which UFBs should be retained after the first generation remain unknown. In cell culture, nitrogen gas nanobubbles in the culture medium are reported to promote cell proliferation (21). To evaluate the physical characteristics of UFBs (N2-UFBs) produced by the generator system used in this study, the UFB concentration in ultrapure water was examined after their generation and within their lifespan. Moreover, the UFB concentration in a culture medium for cell lines was measured after their generation, as well as the growth of the cell lines in different UFB concentrations. In addition, the UFB concentration and size were examined time-dependently using air, carbon dioxide, carbon monoxide, and oxygen to assess the characteristics of various kinds of gases.

Materials and Methods

Preparation of ultrapure water filled with UFBs. The UFB generator system (HMB-H0150+P001, TOSSLEC Corporation Limited, Kyoto, Japan) comprised a circulation tank for the target solution, a pump that circulates the target solution with an electric motor, a pressurized melting device for the choice gas, an ultrasonic irradiation crusher, and a cooling mechanism for the circulation tank using chiller control. Figure 1 shows a schematic of the solution circulation during UFB generation. First, the tank is filled with a particular amount of the target solution required to circulate the system. Second, the solution is continuously circulated using an electric motor. Third, the static pressure decreases when the flow velocity of the pumped solution increases through the narrowness of the venturi tube. Once the solution and gas are in the gas-solution mixed phase, the tube is widened again to lower the flow velocity. This increases the static pressure, and the gas-solution mixture is dissolved. A rapid release under atmospheric pressure supersaturates the solution with gas, generating many fine bubbles. Fourth, the fine bubbles in the liquid are broken down into UFBs by circulating the liquid and irradiating the bubbles with appropriate ultrasonic waves. Thus, the cavitation effect, the expansion and contraction of bubbles due to ultrasonic waves, is related to the crushing mechanism. Subsequently, the circulation tank is cooled to an appropriate temperature (20°C). The solution saturated with UFBs generated by the ultrafine generator system is defined as 100% UFB-concentrated liquid. The number of UFBs in the solution increases based on the time taken to complete one cycle. In this procedure, the UFB-saturated solution is stored at 20°C. To limit the loss of UFBs in storage, the UFB solution was stocked in a glass bottle.

Figure 1.
Figure 1.

Schematic illustration of the generator (HMB-H0150+P001) used to generate ultrafine bubbles (UFBs). The UFB generator uses the pressurized dissolving method and ultrasonic irradiation to generate UFBs. The target solution is added into the circulating tank and continuously stirred within the generator using the pump. The UFBs are generated through dynamic cavitation in the fine bubble generator and ultrasonic cavitation using the ultrasonic irradiation unit using various gases. Circulating the target solution increases the UFB concentration.

Measurements of the concentration and size of nitrogen, carbon dioxide, carbon monoxide, and oxygen gas-filled UFBs (N2, CO2, CO, and O2-UFBs) in ultrapure water. The bubble size distribution was identified using a NanoSight instrument (NanoSight NS300; Malvern PANalytical, Malvern, UK). The NanoSight technique, known as nanoparticle tracking analysis (NTA), is a noninvasive technique that utilizes the characteristics of light scattering and Brownian motion to gain insight into the particle size distribution of a sample in a liquid suspension. A prism-edged glass flat, known as an optical flat, is placed in the sample chamber and used to pass a laser beam. The refractive index and angle of incidence of the glass flat are selected such that the beam refracts intensely when it reaches the glass and liquid sample layer interface. Consequently, a compressed beam with a reduced profile and high-power density is generated. Particles in the beam path can be visualized conveniently by introducing a long working distance (×20 magnification) microscope objective to a traditional optical microscope. The particles scatter light, and their movements under Brownian motion can be captured using a charge-coupled device (CCD), electron multiplied CCD, or high-sensitivity complementary metal-oxide semiconductor (CMOS) camera operating at 30 frames per second, mounted on the microscope. The captured video facilitates real-time analysis of the Brownian motion of nanoparticles or UFBs, enabling the computation of bubble size distribution, mean bubble diameter, and bubble number density.

It should be noted that although Brownian motion takes place in three dimensions, the NTA instrument can observe it only in two dimensions. Nonetheless, two-dimensional UFB tracking is performed to calculate the diffusion coefficient of Brownian motion using the well-known Einstein-Stokes equation (24). The UFB concentration and size were measured immediately after opening the lid of the ultrapure water filled with nitrogen, carbon dioxide, carbon monoxide, or oxygen gas. Each sample was examined at least five times. The mean and standard deviation for each sample was calculated.

Preparation of cell medium with UFBs. For cell culture, NCI-H460, a human lung carcinoma cell line, and mouse embryonic fibroblasts (MEFs) were purchased from the American Type Culture Collection (ATCC, Manassas, VA, USA). Dulbecco’s modified eagle medium (DMEM, Cytiva, Tokyo, Japan) was used as a basal medium to culture the NCI-H460 and MEFs. Fetal bovine serum (FBS; Gibco, Thermo Fisher Scientific, Waltham, MA, USA) and antibiotic-antimycotic (Anti-Anti; Gibco, Thermo Fisher Scientific) were used as supplements. After generating MEM using ultrapure water containing N2-UFB, the cell culture medium was prepared by mixing the MEM containing N2-UFB with 10% FBS and 1% Anti-Anti. The samples were categorized into three groups according to the UFB concentration: low-UFB (L-UFB; 1×108/ml), middle-UFB (M-UFB; 5×108/mL), and high-UFB (H-UFB; 4×109/ml).

Cell culture experiments. The cell lines were incubated on a 100-mm plate in 10 ml of UFB-MEM supplemented with 10% FBS and 1% Anti-Anti at 37°C and 5% CO2. Cultures were established with an initial cell count of 1×106 on day 0. The medium was replaced every three days to remove nonadherent cells, and the adherent cells were passaged with TrypLE Express (Gibco, Thermo Fisher Scientific). The number of cells was counted using Luna-FL (Logos Biosystems, Anyang-si, Republic of Korea) on days 3, 6, 9, and 12.

Statistical analysis. The Mann-Whitney U-test and Benjamini-Hochberg method were used for a univariate analysis of the difference in the UFB concentration or size across time and number of cells. p<0.05 was considered statistically significant. GraphPad Prism 8 (GraphPad Software Inc., San Diego, CA, USA) was used to perform the analyses.

Results

The UFB system generated N2-UFBs in ultrapure water (Figure 2). However, no UFBs were detected in ultrapure water using the NanoSight instrument (Figure 2A). When the UFB system was operated for 1 h, the size of the N2-UFBs ranged 115±3.5 nm (mean±standard deviation), and their concentration was 1.74×109±2.41×108/ml (mean±SD). However, when the system was not operational, no UFBs were detected in ultrapure water (Figure 2A, B, and C). When the system was operated for 4 h, the UFB concentration increased to approximately 4.77×109±2.45×108/ml (mean±SD). However, the UFB size was not significantly altered (Figure 2B and C). Similarly, at a 10-hour, the proposed system generated UFBs with a 10×109/ml concentration. The UFB concentration and size in ultrapure water were measured in three independent times for 1 h to evaluate the reproducibility of UFBs after generation. No significant differences in the UFB concentration and size were observed among the three measurements (Figure 2D). The system was also operated for 4 h in the cell culture medium. After generating UFBs, the UFB concentration increased to approximately 5.22×109±1.82×108/ml (mean±SD). However, the UFB size was not significantly altered (Figure 2E). These results indicated that the UFB system can generate almost the same size of UFBs in liquids, such as ultrapure water and cell culture medium, augmenting the number of UFBs in a time-dependent manner within a particular period.

Figure 2.
Figure 2.

Alterations in the UFB concentration or size using the generator (HMB-H0150+P001) in a time-dependent manner. The NanoSight instrument indicates the concentration or size of each UFB at 0, 2, or 4 h using the generator (A, B). The NanoSight instrument is used to measure the hourly changes in the UFB concentration or size in ultrapure water for 4 h (C). In three independent experiments, the UFB concentration and size in ultrapure water is examined for 1 h using the NanoSight instrument (D). The NanoSight instrument is used to measure the hourly changes in the UFB concentration or size in the cell culture medium for 4 h (E). The red circle or error bars indicate the mean or standard deviation. The asterisk indicates p<0.05 vs. the UFB concentration or size at 1 h.

This study aimed to generate N2 gas-filled UFBs (N2-UFBs) in 30 min. The N2-UFB size and concentration were 113.7±2.7 nm (mean±SD) and 5.83×108±6.17×107/ml (mean±SD), respectively (Figure 3A and B). The N2-UFB concentration significantly decreased from 5.83×108±6.17×107/ml (mean±SD) to 1.99×108±4.19×107/ml (mean±SD) 14 d after generation (p<0.05). After 14 d, the N2-UFB concentration did not significantly decrease for the next 6 months (Figure 3B). In contrast, the N2-UFB size significantly increased to 131.7±5.1 nm (mean±SD) 7 d after generation (p<0.05). Subsequently, the N2-UFB size did not significantly increase in a range of less than 150 nm within 6 months (Figure 3B). These results indicated that UFBs can retain stable physical characteristics, including their size and concentration, from two weeks to 6 months after generation.

Figure 3.
Figure 3.

Fluctuations in the UFB concentration or size in the retention period. The fluctuations in the UFB concentration or size are shown for a period of 6 months (A, B). Each red circle or bar indicates the mean or standard deviation on days 1, 7, 14, 21, 28, 60, 90, 120, 150, and 180. The asterisk indicates p<0.05 vs. the UFB concentration or size at one month after the measurement begins.

This study assessed the characteristics of UFBs using air, carbon dioxide, carbon monoxide, and oxygen gas in a time dependent manner. However, carbon dioxide as hydrophilic gas did not generate the expected amount of UFBs. For hydrophobic gases, such as air, carbon monoxide, and oxygen, a significant amount of UFBs were generated as nitrogen in a time dependent manner (Figure 4). These results indicated that the UFB system can generate high UFB concentrations using any hydrophobic gas in a time dependent manner.

Figure 4.
Figure 4.

Alterations in the UFB concentration (A) or size (B) generated by different gases using the generator (HMB-H0150+P001) in a time-dependent manner. The hourly changes in the UFB concentration or size are shown for 4 h for UFBs filled with nitrogen, air, oxygen, carbon monoxide, or carbon dioxide. The asterisk indicates p<0.05 vs. the N2-UFB concentration or size at each generation time.

The increase in the number of cells was examined through image analysis using Luna-FL to evaluate the effects of UFBs on cell proliferation. Figure 5 shows the number of cells on days 0, 3, 6, 9, and 12 with control, L-UFB (approximately 1×108/ml), M-UFB (approximately 5×108/ml), and H-UFB (approximately 4×109/ml). Significant increases in the number of cultured cells (NCI-H460 and MEF) were observed in the L-UFB and M-UFB groups compared with those in the control group. Conversely, the number of cultured cells (NCI-H460 and MEF) in the H-UFB group decreased significantly compared with that in the control group on day 12.

Figure 5.
Figure 5.

Number of cells in culture medium containing UFBs. The number of cells is shown every 3 days, up to 12 days. The media are divided into three groups according to the UFB concentration: Low-UFB (L-UFB; 1×108/ml), Middle-UFB (M-UFB; 1×109/ml), and High-UFB (H-UFB; 5×109/ml). *p<0.05 vs. control.

Discussion

This study demonstrated the generation of UFBs filled with different hydrophobic gases in ultrapure water using a generator system (HMB-H0150+P001). The results demonstrated that the UFB concentration in ultrapure water increased as the generator system worked in a time-dependent manner. The UFB concentration and size were stable from two weeks after the UFB generation up to 6 months.

This study also highlighted that the number of UFBs increased because the generator system (HMB-H0150+P001) efficiently generated UFBs when the solution was circulated using hydrodynamic and ultrasonic cavitation. The reactive free radicals in liquid were generated from thermal decomposition and bubble collapse during the UFB generation. These free radicals were adsorbed onto the bubble interface, defining the electrical properties of UFBs (26). However, hydrodynamic cavitation induced high temperature and pressure inside the bubble cavity, resulting in the thermal decomposition of water vapor to generate OH radicals (8, 27). The generator system comprised hydrodynamic and ultrasonic cavitations. The UFB-filled solution in the generator system was cooled at 20°C. Therefore, any UFB-filled solution generated by the generator system and no abundant free radicals would theoretically be harmless for cultured cells, plants, and animals.

The UFB concentration temporarily decreased, and the UFB size increased in the first two weeks of generation. Theoretically, the generated UFBs are expected to disappear in a short time. The UFB lifespan is approximately 150 nm. Although this is quite short according to the Epstein-Plesset theory, in this study, no significant changes in the UFB concentration and size were observed from two weeks after their generation until 6 months. As described by Kanematsu et al., the storage of UFBs in a glass bottle was relatively stable for 12 months (28). However, the stabilization mechanism of UFBs remains unclear. According to previous studies, nine models for implementing the stabilization mechanisms in UFBs have been proposed. These models are primarily based on the following parameters: 1) skins of varying permeability, 2) dissolution of coated microbubbles, 3) ultrasonic cavitation in tap water, 4) submicrometric bubbles with long life, 5) bubston structure of water and adequate solution of electrolytes, 6) diffuse shielding, 7) bubble formation in water, 8) stabilization of boiling nuclei by insoluble gas, and 9) advanced dynamic-equilibrium model (29-39). Yasui et al. reported that when the UFB size is approximately 150 nm, the UFBs become stable because more than 50% of the UFB surface coverage should be formed by hydrophobic substances (40). In this study, the UFB size was approximately 150 nm in steady-state, consistent with that reported by Yasui et al. (40, 41).

Previous studies have reported that UFBs could be effective or useful for cultured cells, plants, and animals. Consequently, the UFB mechanism is transfected into living cells. In general, living cells exhibit endocytosis as an intracellular import mechanism (42). Extracellular vesicles, which secrete particles with size ranging from 50 to 150 nm, are fetched by cells surrounding them and carried to the nucleus, Golgi apparatus, endoplasmic reticulum, and mitochondria, indicating that signal transduction can be activated in these living cells (42, 43). Using nitrogen gas, the UFB concentration influences the proliferative effects of cultured cells, suggesting that the stable UFB size may be incorporated into the cells through cellular endocytosis. Moreover, the UFBs made with various hydrophobic gases can adequately regulate cell behavior through cellular signal transduction.

Conclusion

The generator system (HMB-H0150+P001) can produce UFBs of extremely high concentrations using various hydrophobic gases at low temperatures without intense heat generation. The target UFB concentration can be retained for long periods in any liquid. In addition, the medium containing UFBs can be used for cell culture, and there is an adequate UFB concentration for the growth of adherent cells. The optimum condition can be explored for various biological fields using different hydrophobic gases in microorganisms, cells, plants, fish, and animals. These results indicate that the generator system (HMB-H0150+P001) can be used to generate UFBs to induce innovative biological events.

Acknowledgements

We appreciate the excellent technical assistance from Ms. Shiori Imi, Department of Obstetrics & Gynecology, Faculty of Medicine, Fukuoka University. This work was supported in part by the Fukuoka University grant to T. Hirakawa (grant number 226004), a Grant-in-Aid from the Japan Agency for Medical Research and Development (Tokyo, Japan) to S. Miyamoto (grant number 210138), a Grant-in-Aid from the Chugai Pharmaceutical Co. Ltd (Tokyo, Japan) to S. Miyamoto (grant number 210268), and a Grant-in-Aid from the Tsumura & Co. (Tokyo, Japan) to S. Miyamoto (grant number 210252). The funding sources had no involvement in any aspect of the study, including the design, data collection and analysis, report writing, or submission of the article for publication. We thank Editage (https://www.editage.jp/) for their English language editing services.

Footnotes

  • Authors’ Contributions

    S.M. and T.H. initiated and conceptualized the research. W.N., T.O., Y.N., I.F., and J.M. devised the generator system (HMB-H0150+P001) and executed the assembly and upkeep of the machinery. Y.N., D.U., and K.M. executed the generation of UFBs using the generator system (HMB-H0150+P001). W.N., T.B., F.Y., and S.Y. appraised the UFB using NanoSight. K.N. and K.H. analyzed the data. T.H. participated in every experiment. S.M. envisioned the study and participated in its formulation and oversight. T.H. and S.M. composed and revised the manuscript. All Authors deliberated on the results and provided adequate input for preparing the manuscript.

  • Conflicts of Interest

    The Authors declare no conflicts of interest.

  • Received May 13, 2023.
  • Revision received July 27, 2023.
  • Accepted August 3, 2023.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Physical Properties of Ultrafine Bubbles Generated Using a Generator System
SHINGO MIYAMOTO, TOYOFUMI HIRAKAWA, YUKIKO NOGUCHI, DAICHI URUSHIYAMA, KOHEI MIYATA, TSUKASA BABA, FUSANORI YOTSUMOTO, SHIN’ICHIRO YASUNAGA, KAZUHIKO NAKABAYASHI, KENICHIRO HATA, WATARU NAKAGAWA, TOSHIHIRO OTSUKA, YOSHIKO NOZAWA, IPPEI FURUHATA, JITSUO MIKASA
In Vivo Nov 2023, 37 (6) 2555-2563; DOI: 10.21873/invivo.13363
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