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. 2023 Jun 26;23(13):5981–5988. doi: 10.1021/acs.nanolett.3c01166

Photonic Lithotripsy: Near-Infrared Laser Activated Nanomaterials for Kidney Stone Comminution

Ian Houlihan †, Benjamin Kang †, Smita De ‡,§,*, Vijay Krishna †,∥,*
PMCID: PMC10348310  PMID: 37358929

Abstract

graphic file with name nl3c01166_0005.jpg

Near-infrared activated nanomaterials have been reported for biomedical applications ranging from photothermal tumor destruction to biofilm eradication and energy-gated drug delivery. However, the focus so far has been on soft tissues, and little is known about energy delivery to hard tissues, which have thousand-fold higher mechanical strength. We present photonic lithotripsy with carbon and gold nanomaterials for fragmenting human kidney stones. The efficacy of stone comminution is dependent on the size and photonic properties of the nanomaterials. Surface restructuring and decomposition of calcium oxalate to calcium carbonate support the contribution of photothermal energy to stone failure. Photonic lithotripsy has several advantages over current laser lithotripsy, including low operating power, noncontact laser operation (distances of at least 10 mm), and ability to break all common stones. Our observations can inspire the development of rapid, minimally invasive techniques for kidney stone treatment and extrapolate to other hard tissues such as enamel and bone.

Keywords: lithotripsy, carbon nanomaterials, gold nanomaterials, calcium oxalate, noncontact laser, low intensity laser

Kidney stones, also known as nephrolithiasis, are increasingly prevalent, with 1 in 9 individuals being affected in the U.S., and the prevalence expected to increase to 13% by 2030.1,2 Kidney stones are mineral-based precipitates that develop in the collecting system (pelvis and calyces) of the kidney and are associated with crippling pain, severe infection, kidney damage, and even death.3,4 When small enough (<2 mm), stones can travel through the ureter and pass into the bladder.5 However, larger stones can become obstructed in the ureter, causing the pain commonly associated with stones. The most common stone treatments include laser lithotripsy by ureteroscopy, during which stones are visualized with a camera and comminuted (lithotripsy) using contact lasers (and may be removed with small baskets), and extracorporeal shock wave lithotripsy (ESWL), where external acoustic shockwaves are focused on stones to produce fragments that the patient must then pass.6

Clinical laser lithotripsy utilizes a high-powered (up to 120 W) pulsed holmium yttrium-aluminum-garnet (Ho:YAG) laser or a thulium fiber laser operating at a wavelength of 2120 or 1920 nm, respectively, both of which have very high water absorption.7−10 Laser lithotripsy occurs from laser energy absorption by water molecules surrounding stones that results in rapid vaporization, expansion, and cavitation, releasing energy that promotes crack formation and propagation, leading to fatigue and breakdown. Studies on human kidney stones irradiated with Ho:YAG laser in aqueous systems have proposed contributions of photothermal and thermomechanical mechanisms for comminution.11−18 Stone comminution with laser lithotripsy requires contact of the laser fiber tip with stones to reduce the risk of undesirable kidney damage.3,19

Photonic nanomaterials that are activated by deep-tissue-penetrating near-infrared lasers with minimum water absorption have been widely reported for their favorable photothermal and photoacoustic properties in a variety of different medical applications.20,21 The photonic nanomaterials are either carbon-based, such as fullerenes, carbon nanotubes, and graphene, or gold-based, such as nanoshells, nanorods, and nanostars. The carbon- and gold-based photonic nanomaterials have been utilized for cancer treatment, drug delivery, treatment of biofilms and as contrast agents.21−28 The photothermal and photoacoustic energies generated from these nanomaterials have been reported to provide noninvasive and targeted destruction of soft tissues, such as solid tumors.29−31 However, there are no reports on utilizing these photonic nanomaterials for the treatment of hard tissues such as bones and kidney stones. Hard tissues have an elastic modulus on the order of GPa (e.g., 25 GPa for kidney stones) whereas soft tissues have elastic modulus on the order of kPa to MPa (e.g., 40 MPa for prostate tumor).32−36 Photonic nanomaterials were not expected to affect hard tissues, as they have 3 orders of magnitude higher mechanical strength than soft tissues.

In this work, we expand the application of photonic nanomaterials to hard tissue and demonstrated a novel method, photonic lithotripsy, for kidney stone treatment. Carbon (fullerenes, nanotubes, and graphene)- and gold (nanoshells and nanorods)-based photonic nanomaterials were selected based on their commercial availability, size, shape (0D, 1D, and 2D), composition, and biocompatibility. When the photonic nanomaterials are in contact with kidney stones, low-intensity (<5 W) laser irradiation from a distance activates the nanomaterials that directly transfer photothermal and photoacoustic energy to the stones, causing photothermomechanical stress leading to comminution (Figure 1). We show that photonic lithotripsy can comminute different types of human kidney stones in vitro with high efficacy. The efficacy of stone comminution is dependent on the size and photonic properties of the nanomaterials. Further, we have developed a method to characterize individual stones before and after photonic lithotripsy with FTIR, μCT, and SEM, which we utilize to confirm the contribution of photothermal energy to stone failure. The novel use of photonic nanomaterials in this study can enable minimally invasive kidney stone treatment and expand the application of these materials to other hard tissues.

Figure 1.

Figure 1

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Photonic lithotripsy concept. Kidney stones are coated with photonic nanomaterials. Irradiation with a near-infrared laser activates the nanomaterials that directly transfer photothermal and photoacoustic energy to stones, causing mechanical stress that ultimately leads to failure and creates stone debris.

Characterization of Photonic Nanomaterials

We have discovered that photonic nanomaterials can break down human kidney stones with low-powered near-infrared lasers. We tested different carbon- and gold-based commercial photonic nanomaterials. The size and morphology of the nanomaterials were characterized by electron microscopy (Figure 2A) and dynamic light scattering (Figure 2B). High-resolution transmission electron microscopy (HR-TEM) was employed only for the smallest nanomaterial, polyhydroxy fullerene (PHF), which was predominantly used in this study. The HR-TEM image of PHF shows clusters that are 3.4 ± 0.5 nm in size, which is very close to the hydrodynamic size of 8.3 ± 2.2 nm. Scanning electron microscopy (SEM) of carboxylate-functionalized multiwalled carbon nanotubes (MWNT) shows filaments with a thickness of 14.4 ± 4.45 nm and several micrometers in length. The hydrodynamic size of the MWNT is 321 ± 58 nm. Graphene oxide sheets appear as agglomerates with a crumpled morphology and an average hydrodynamic size of 485 ± 106 nm. Gold nanoshells (AuNS) are smooth spherical particles with a size of 160 ± 4.8 nm, which is close to their hydrodynamic size of 154 ± 4 nm. The SEM of gold nanorods (AuNR) exhibits mostly rod-shaped material (thickness of 49 ± 5 nm and length of 12 ± 0.8 nm) with a few spheres (indicated by arrows), and the hydrodynamic size is 5.28 ± 0.39 nm. It is important to note that the dynamic light scattering technique is not suitable for MWNT and AuNR due to the high aspect ratio and the underlying assumption of spherical particles used for calculating the hydrodynamic particle size. This is also a limitation for graphene; however, the hydrodynamic size may represent crumpled particles.

Figure 2.

Figure 2

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Photonic nanomaterial characterization. (A) Carbon- and gold-based photonic nanomaterials utilized in this study. HR-TEM of polyhydroxy fullerenes (PHF) and SEM images for carboxylated multiwalled carbon nanotubes (MWNT), graphene oxide (graphene), gold nanoshells (AuNS) and gold nanorods (AuNR). (B) Hydrodynamic size of nanomaterials measured with dynamic light scattering. (C) Visible and NIR absorption spectra for photonic nanomaterials measured at a concentration of 0.01 mg/mL. (D) Photothermal efficiency and maximum temperature reached with a 785 nm laser. (E) Photothermal efficiency and maximum temperature reached with a 1320 nm laser. Photothermal efficiencies were measured at the same laser absorptions (I/I0), and the concentrations were determined in a separate experiment (Figure S1).

The near-infrared (NIR) absorption spectra for all five nanomaterials obtained at a concentration of 0.01 mg/mL are shown in Figure 2C. Gold-based nanomaterials (AuNS and AuNR) exhibit a broad absorption peak at 808 nm with full widths at half-maximum of 301 and 142 nm for AuNS and AuNR, respectively, which is expected based upon their design. Importantly, none of the carbon nanomaterials tested have any peaks in the NIR region. Two different laser wavelengths used in this study (presented as vertical lines in the graph) were chosen, as they had a low level of absorption by the kidney tissue and were in two different biological NIR windows.37,38 The photonic nanomaterials were further characterized for their photothermal conversion efficiency (i.e., efficiency of converting light energy to thermal energy or heat) with both 785 and 1320 nm lasers following our previously reported protocol.39 In order to compare different photonic nanomaterials, laser absorption was measured at different concentrations, and the concentrations with similar laser absorption (variation less than 2%) were selected (Figure S1). The photothermal efficiencies are presented as bar graphs in Figure 2D,E, and the maximum temperature attained after 30 min irradiation is depicted by the hollow squares on each graph. The photothermal efficiency of AuNSs with a 785 nm laser is 41%, which is consistent with the literature,40 and the maximum temperature attained was 62.5 ± 2 °C, both values significantly lower (p = 0.05; Figure S2) than those for all other nanomaterials tested. Interestingly, no significant differences in the photothermal efficiency or maximum temperature achieved with different nanomaterials were observed with the 1320 nm laser. The similarity in maximum temperature could be due to higher absorption by water.41

Human Kidney Stone Comminution with Photonic Nanomaterials

The ability of PHF as a photonic nanomaterial for comminution was evaluated with human kidney stones of different compositions (Figure 3A). The stones were first rehydrated in simulated urine for 24 h before experiments. Control experiments with 9 min laser irradiation did not break any stones. For photonic lithotripsy, 30 μL of 10 mg/mL PHF was pipetted on top of the stones and immediately irradiated with a 785 nm laser at 2 W for 9 min from a distance of approximately 10 mm. PHF successfully fragmented different types of kidney stones. Most importantly, PHF was able to break down calcium oxalate monohydrate stones, which are the hardest type of kidney stone34,42,43 and are resistant to clinical shockwave lithotripsy.44

Figure 3.

Figure 3

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Kidney stone comminution with photonic nanomaterials. (A) Photonic lithotripsy of different types of kidney stones with PHF and a 2 W 785 nm laser. COM stones contain 60% calcium oxalate monohydrate, 30% calcium oxalate dihydrate, and 10% uric acid. COD stones contain 60% calcium oxalate dihydrate, 30% calcium oxalate monohydrate, and 10% uric acid. CaP stones contain 80% calcium phosphate, 10% calcium oxalate monohydrate, and 10% calcium oxalate dihydrate. Cys stones contain 70% cystine and 30% calcium phosphate. UA stones contain 100% uric acid. Str stones contain 50% struvite, 40% uric acid, and 10% calcium phosphate. (B) Photonic lithotripsy of COM stones with different nanomaterials and a 2 W 785 nm laser. Laser alone does not damage the stones. (C) Percentage of different COM stones comminuted with different nanomaterials and 2 W 785 nm laser. (D) Percentage of different COM stones comminuted with different nanomaterials and a 4 W 1320 nm laser. (E) Comparison of stone comminution for carbon-based and gold-based nanomaterials at two different laser wavelengths for COM stones.

Further studies were conducted with stones composed of predominantly calcium oxalate monohydrate (60% calcium oxalate monohydrate, 30% calcium oxalate dihydrate, and 10% uric acid), which is the most common kidney stone found in clinical practice.45−47 Photonic lithotripsy was performed with each nanomaterial on 10 stones with 785 and 1320 nm lasers. The pre (top) and post (bottom) laser irradiation images of stones treated with different nanomaterials and the 785 nm laser are shown in Figure 2B. Control experiments with laser irradiation alone did not break any stones. All tested photonic nanomaterials were able to break down calcium oxalate kidney stones. The time taken to break the stones was further divided into three 3 min intervals (Figure S3). All nanomaterials fragmented at least 7 out of 10 stones in first 3 min of irradiation with a 785 nm laser. Only PHF, AuNS, and AuNR were able to fragment all ten stones, whereas MWNT and graphene oxide broke 8 and 7 stones in 9 min, respectively (Figure 3C). Since the photothermal efficiency and maximum temperature achieved with MWNT and graphene are significantly higher than those of AuNS, the observed lower efficacy with these two carbon nanomaterials can be explained based on their size and contact with kidney stones. All three dimensions of PHF, AuNS, and AuNR are in the nanoscale with sizes less than 100 nm, whereas MWNT and graphene oxide have at least one dimension in the micrometer scale, which reduces the contact with irregular-shaped kidney stones, resulting in lower efficacy for photonic lithotripsy. A more intimate contact between the stone and nanomaterial would, in theory, result in lower energy transfer losses and ensure a more effective comminution.

With a 1320 nm laser, only PHF was able to fragment 100% of the stones tested (Figure 3D). The trend in performance of carbon nanomaterials was similar to that at 785 nm with MWNT and graphene breaking 90% and 70% of the stones, respectively. The lower comminution efficacy can again be explained based on reduced contact between MWNT and graphene with the kidney stones. Interestingly, AuNS and AuNR broke less than 50% of the stones with the 1320 nm laser. Figure 3E compares the fragmentation of the same batch of kidney stones between carbon- and gold-based nanomaterials at two different laser wavelengths. Gold-based nanomaterials are designed for 808 nm, and this could explain their lower performance against carbon nanomaterials with the 1320 nm laser. Another explanation for the better performance of PHF could be due to the higher concentration utilized (Figure S1), which results in a greater number of particles in contact with the stones.

Notably, kidney stones after comminution with photonic lithotripsy exhibited color changes, as seen in Figure 3A,B. A significant amount of black coloration was observed, which could be due to charring of the organic components of the kidney stones as well as carbon nanomaterials, as stones treated with carbon nanomaterials had more black coloration than gold-based nanomaterials. A smaller amount of white pigmentation was also observed and could indicate thermal degradation or restructuring of calcium oxalate crystals. Interestingly, white coloration was observed more with the 1320 nm laser (Figure S4) than with the 785 nm laser, suggesting a stronger photothermal contribution for comminution as noted below.

Mechanistic Insights for Photonic Lithotripsy

In order to gain a deeper understanding of the mechanism of failure in photonic lithotripsy, microcomputed tomography (μCT) and SEM were utilized to analyze the changes in the stone pre- and post-irradiation with the 1320 nm laser. Previous studies have also shown μCT to be a powerful technique for analyzing kidney stones and their failure mechanisms.48,49 A new method was developed to analyze the same stone pre- and post-irradiation with μCT and SEM (Figure S5). Each stone was fixed in a 3D-printed holder (10 × 10 mm) with double-sided tape to ensure the orientation of the stone did not change during lithotripsy. The stones were imaged with SEM and μCT and then rehydrated in 2 mL of simulated urine for lithotripsy experiments, which were conducted as mentioned above. After the laser irradiation, utmost care was taken to avoid stone fragments from falling apart for further analyses. The μCT and SEM images of one calcium oxalate monohydrate stone before and after photonic lithotripsy with PHF and a 1320 nm laser are presented in Figure 4, and a video of stone fragmentation during lithotripsy is provided in the Supporting Information. During photonic lithotripsy, the color of the stone surface at the site of irradiation turned darker first and then started to glow red and increased in area. Within 10 s, the glowing surface turned white and expanded, creating cracks that traveled through the core and fragmented the stone. The μCT images clearly show cracks running from the surface to the core from different directions (yellow arrows in Figure 4A), suggesting that the crack formation and propagation are a result of both thermal and mechanical stress. The surface area of the stone was also determined from the μCT data, which increased after lithotripsy (Figure S6) and was consistent with the observed expansion and fragmentation. SEM imaging was conducted under a low vacuum to prevent extreme dehydration that could stress the stones and increase the chances of failure. The SEM morphology of kidney stones (Figure 4B) consists of amorphous (green oval) phases as well as whewellite (purple oval) and weddellite (blue oval) crystal phases, consistent with the literature.50,51 After photonic lithotripsy, significant microstructural changes including micrometer-scale cracks (yellow ovals) and surface restructuring (dashed yellow circles) were clearly visible. The sharp crystal features were no longer visible, and the surface appeared flattened, suggesting changes in crystal structure. This observation is supported by a previous report on microstructural changes in calcium oxalate to calcium carbonate in ashed oak leaves, where crystals transform into fused masses upon heat treatment as well as the breakdown of the crystals into smaller fragments and the loss of druses from the original untreated sample.52 To confirm the thermal changes occurring at the surface of kidney stones, a thermal camera was employed to determine the surface temperature during photonic lithotripsy with a 1320 nm laser. A representative thermal image of a stone during lithotripsy after 3 min of irradiation is shown in Figure 4C. The peak temperature observed ranged from 528 to 660 °C, which was the upper limit of detection for the thermal camera. It is possible that the peak surface temperature was higher than 660 °C. Thermal decomposition of calcium oxalate to calcium carbonate in kidney stones is reported to occur in the range of 470–496 °C.53,54 Thermal decomposition has also been observed with holmium:YAG laser lithotripsy.55 The surface chemical changes from high temperatures were confirmed by vibrational spectroscopy. The FTIR of a calcium oxalate kidney stone (Figure 4D) shows three major peaks at 1611, 1313, and 778 cm–1 corresponding to C=O stretch, C–O stretch, and C–C stretch, respectively, and is consistent with the literature.50,53,56,57 After photonic lithotripsy, the white surface was scraped for analysis and compared with standard calcium carbonate. The FTIR spectra clearly show three additional peaks at 1394, 872, and 712 cm–1 corresponding to calcium carbonate peaks. The activation energy for calcium oxalate monohydrate to calcium carbonate has been reported to be in the range of 180–290 kJ/mol,58 which translates to approximately 140 J for a 50 mg stone. The photothermal energy generated by PHF (photothermal efficiency of 70%) with a 1320 nm laser at 4 W and 3 min of irradiation is approximately 500 J, which is significantly higher than the upper limit required for thermal decomposition of calcium oxalate monohydrate. These observations suggest that photonic lithotripsy causes photothermal decomposition and mechanical stress for fragmentation. It should be noted that the stones were tested without being immersed in a liquid environment, which could dissipate heat and minimize photothermal damage.

Figure 4.

Figure 4

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COM stone characterization before and after photonic lithotripsy with PHF and a 1320 nm laser. (A) Microcomputed tomography images showing axial, coronal, and sagittal views of stone before and after photonic lithotripsy. Yellow arrows indicate cracks from the surface to the core of the stone. (B) SEM images of the same stone before and after photonic lithotripsy at two different magnifications: green oval, amorphous region; purple oval, whewellite structure; blue oval, wedellitte structure; yellow ovals, microcracks; yellow dashed circle, surface restructuring. (C) Thermal image of the stone during photonic lithotripsy. The maximum detection threshold of the camera is 660 °C. (D) FTIR spectra of the stone before and after photonic lithotripsy and standard calcium carbonate. Dashed rectangles indicate that new peaks arising from lithotripsy are similar to those from calcium carbonate.

In summary, we have developed a novel method for kidney stone comminution with photonic nanomaterials. Near-infrared activated carbon- and gold-based nanomaterials were utilized, for the first time, to break down different types of kidney stones, including the hardiest calcium oxalate monohydrate stones. The mechanism of stone failure was proposed to be a combination of photothermal and mechanical stress. Finally, we presented evidence for the surface thermal decomposition of calcium oxalate crystals to calcium carbonate with photonic lithotripsy. This work on using photonic nanomaterials for breaking stones can be extended to new applications with hard tissues, such as bones, and paves the way for a new method to treat nephrolithiasis.

Acknowledgments

The authors acknowledge the financial support from the Lerner Research Institute’s Accelerator Award, Cleveland Clinic Caregiver Catalyst Award, Lerner Research Institute’s seed funds, and NIH U2C support (TL 1DK132770). Any opinions, findings, conclusions or recommendations expressed herein are those of the author(s) and do not necessarily reflect the views of the funders. SEM was carried out at the Swagelok Center for Surface Analysis of Materials. I.H. acknowledges assistance from Dr. Tugce Karakulak Uz for the SEM imaging of the nanomaterials. I.H. acknowledges the training and assistance of Dr. Charlie Androjna with μCT in the Small Animal Imaging Core at the Lerner Research Institute. I.H. also acknowledges the help of Alan Chen for the editing of the supplementary video.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.nanolett.3c01166.

  • Materials and methods, laser absorption of the nanomaterials, statistical analysis of photothermal efficiency and maximum temperatures, stone fragmentation by time period of laser irradiation, images of stones irradiated with 1320 nm laser, schematic of the protocol for analyzing a single kidney stone, surface area data from μCT (PDF)

  • Video of stone fragmentation during lithotripsy (MP4)

Author Contributions

V.K., S.D., and I.H. conceived and designed the experiments and analyzed the data. S.D. obtained access to human kidney stones. I.H. and B.K. performed the photonic lithotripsy experiments and data analysis. The manuscript was written by I.H., S.D., and V.K.

The authors declare the following competing financial interest(s): I.H., S.D., and V.K. are co-inventors in a patent application for this technology.

Supplementary Material

nl3c01166_si_001.pdf (965.2KB, pdf)
nl3c01166_si_002.mp4 (3.5MB, mp4)

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