Research Article www.acsami.org
New Generation of Gold Nanoshell-Coated Esophageal Stent: Preparation and Biomedical Applications Jibin Song,† Hao Hu,‡ Chao Jian,‡ Kaichun Wu,‡ and Xiaoyuan Chen*,† †
Laboratory of Molecular Imaging and Nanomedicine (LOMIN), National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health, Bethesda, Maryland 20892, United States ‡ Sate Key Laboratory of Cancer Biology & Xijing Hospital of Digestive Diseases, Fourth Military Medical University, Xi’an, China S Supporting Information *
ABSTRACT: Esophageal cancer is one of the six most common cancers in the world, constituting ∼7% of the gastrointestinal cancers. Esophageal stents can be inserted into the esophagus to open the pathway as a palliative treatment for advanced esophageal cancer. For the treatment of esophageal cancer, a series of anticancer drug-loaded stents such as paclitaxel or 5fluorouracil/esophageal stent combinations have been prepared by covering a nitinol stent with a polymer or hydrogel shell. For the first time, we developed a gold nanoshell (AuNS)-coated stent with high photothermal efficiency and used in the repetitive photothermal therapy of esophageal cancer. The functionalized stent was prepared by using surface-coated polydopamine as the Au3+ anchor and template. The thickness of the AuNS can be easily adjusted by controlling the reaction time and amount of Au3+. The AuNS-coated stent efficiently increased the temperature of pork and porcine intestines irradiated with a near-infrared (NIR) laser. The deep penetration of the NIR laser and excellent stability of the stent provide opportunity for the clinical applications of the newly functionalized stent. In vitro toxicity experiments showed excellent biocompatibility and safety of this device. Compared with bare metal stent, AuNS-modified stent exhibits great potential to open the duct passageway and suppress tumor growth in future clinical applications. KEYWORDS: gold nanoshell, dopamine, stent, cancer, photothermal therapy, NIR laser
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INTRODUCTION In clinical medicine, a stent is a plastic or metal tube inserted into a duct or the lumen of an anatomic vessel to keep the passageway open.1,2 Diverse stents are widely used for different purposes; for example, vascular and biliary stents expand coronary arteries and allow the flow of urine between the bladder and kidneys, respectively.3,4 Esophageal stents are used for the palliative treatment of advanced esophageal cancer.5,6 Besides the basic function of the sent, a series of anticancer drug-loaded stents such as paclitaxel or 5-fluorouracil/ esophageal stent combination have been prepared by covering a nitinol stent with a bilayer polymer shell.7,8 These drugloaded stents exhibited a prolonged and sustained unidirectional cancer drug release behavior.9,10 In vivo experiments showed that the concentration of drug in the stent-contacted tissues was significantly higher than the other organs, for example, the heart, spleen, liver, kidneys, lung, and blood.11,12 Therefore, drug-loaded stents can be used for localized release of drugs and tumor chemotherapy.1−4 This is a highly nontoxic and efficient potential treatment modality for patients with esophageal cancer. However, anticancer drugs kill cancer cells as well as normal cells at the same time, thus usually causing some unpleasant side effects.2 © 2016 American Chemical Society
Recently, photothermal therapy (PTT) has been widely investigated and used for cancer therapy with high efficiency and accuracy.13 Gold nanomaterials are one of the most widely used photothermal agents. They have high photothermal conversion efficiency and are safe for biomedical applications.14,15 Under near-infrared (NIR) laser irradiation, only the temperature of gold nanocrystal-treated tissue is significantly increased, thus leading to ablation of the tissue.16 Gold nanoshells (AuNS) are broadly used gold nanomaterials, and they create strong local electromagnetic fields at the nanoshell surface at resonance, leading to high absorption of light and heat-transfer efficiency.17 For example, thin AuNS-coated silica gold nanoparticles have been used for the PTT of cancer cells and tumors.15,18,19 Importantly, the temperature increase and irradiated region of the tumor can be easily adjusted by the laser power density and spot size, allowing for accurate therapy.20−24 Here, for the first time, we report a new type of AuNS-coated esophageal stent with high photothermal effect using a PDAReceived: July 23, 2016 Accepted: September 29, 2016 Published: September 29, 2016 27523
DOI: 10.1021/acsami.6b09104 ACS Appl. Mater. Interfaces 2016, 8, 27523−27529
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Figure 1. Schematic illustration of the preparation of gold nanoshell-coated stent using poly(dopamine) (PDA) as an anchor to adsorb and reduce Au3+.
based approach as shown in Figure 1. The stent was first coated with a layer of PDA, which can be used as a template and an anchor to adsorb Au3+, followed by the formation of AuNS using ethylene glycol as a reducing agent.25−28 The thickness of the AuNS can be easily adjusted by the amount of Au3+ and reaction time. Mussel-inspired self-polymerized PDA is used for adhesion on any inorganic and organic substrates, facilitating robust binding on different types of stents such as plastic and metal stents.27 It is possible to prepare functionalized stents on a large scale because the formation of a PDA layer is a one-step reaction and requires only a short time to complete the process. The photothermal experiments for pork and porcine intestines treated with a AuNS-coated stent and NIR laser showed high photothermal effect and deep penetration. Importantly, the laser irradiation area and depth could be adjusted by the laser spot size and intensity, thus allowing accurate PTT and avoiding severe damage to the normal tissue at the esophagus stent implantation location. This new device designed to achieve the localized and accurate PTT of esophageal cancer was evaluated with respect to its photothermal effect, stability, and fat-heating behavior.
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(Center Valley, PA). Ultrapure water (18.2 MΩ·cm) was purified using a Sartorius AG arium system and used in all experiments. Scanning electron microscopy images were obtained on a Hitachi SU70 Schottky field emission gun scanning electron microscope (FEGSEM). Fluorescence images of the cell were collected using a Photometrics CoolSNAP-cf cooled CCD camera. Preparation of Gold Nanoshell-Coated Stent. To synthesize PDA-coated stent, one stent was put in 400 mL of 10 mM TRIS buffer (pH 8.5) under stirring. Dopamine (2 mg/mL) was added into the solution. The reaction was maintained under stirring for 8 h. The PDA-coated stent was washed with water and added into 400 mL of ethylene glycol, followed by the addition of HAuCl4 solution. After reaction for 1 h at 100 °C, the AuNS-coated stent was washed by water. The AuNS-coated stent nitinol wire was prepared by using a method similar to that used in the preparation of the AuNS-coated stent. Photothermal Effect of the AuNS-Coated Stent Irradiated with NIR Laser. AuNS-coated stent in aqueous solution was irradiated with an 808 nm laser at different power densities for different periods of time. The temperature increases and thermal images of the stent were examined by using an infrared thermal camera. The photothermal performance of the AuNS-coated stent was also tested under the same conditions. As a control experiment, the stent without gold nanoshell coating was also irradiated with NIR laser. Photothermal Therapy of Cancer Cells with AuNS-Coated Stent Wire. U87MG cells were incubated in 24-well plates at a density of 4.0 × 104 cells per well and incubated for 1 h. AuNS-coated stent wire was then placed in the well, followed by laser irradiation at a power density of 0.25 W/cm2 for 3 min. After incubation for 12 h, cells
EXPERIMENTAL SECTION
Materials and Equipment. Nitinol stents were purchased from Micro-Tech Co., Ltd. (Nanjing, China), gold(III) chloride trihydrate (HAuCl4·3H2O), propidium iodide (PI), ethylene glycol, and dopamine were purchased from Sigma-Aldrich (St. Louis). Tris(hydroxymethyl)aminomethane (TRIS) was obtained from J.T. Baker 27524
DOI: 10.1021/acsami.6b09104 ACS Appl. Mater. Interfaces 2016, 8, 27523−27529
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Figure 2. FE-SEM images of the stent wire before (a) and after being coated with PDA (b), and gold nanoshell (c) and (d) at higher magnification. FE-SEM images of the stent wire coated with small gold nanoparticles (e) and complete gold nanoshell (f). Photographs of one esophageal stent before (g) and after (h) being coated with gold nanoshell. were stained with PI and calcein AM for 10 min, followed by washing with phosphate buffered saline (PBS). The cell fluorescence images were recorded using a Photometrics CoolSNAP-cf cooled CCD camera. Photothermal Performance of the AuNS-Coated Stent for the Pork, Pig Intestines, and Tumor. AuNS-coated stent wire was placed on one piece of pork and then irradiated with NIR laser at the power densities of 0.25 and 0.5 W/cm2 for 5 min, respectively. The infrared camera was used to record the infrared images and the temperature increase of the laser-irradiated area. To further investigate the photothermal penetration depth of the functionalized stent, AuNS-coated stent wire was inserted into one piece of pork, followed by irradiation with NIR laser at a power density of 0.25 W/cm2 for 5 min. Infrared camera was employed to test the laser irradiation depth and temperature increase of the irradiated area. To simulate the esophageal environment, AuNS-coated esophageal stent was implanted into one pig intestine. NIR laser was used to irradiate the intestine with different laser spot sizes at a power density of 0.25 W/cm2. When the U87MG tumor size reached ∼70 mm3, two AuNS-coated stent wires were inserted into the tumor (n = 3 mice per group). Afterward, the whole tumor was irradiated with 808 nm laser at a power density of 0.25 W/cm2 for 5 min. The tumor size was measured every 2 days.
with the bare stent wire with rough surface, a thick smooth layer of PDA was observed on the surface of the stent wire, as shown in Figure 2a,b. The presence of PDA layer was further verified by FTIR spectra of the PDA-coated stent wire, as shown in Figure S3 of the Supporting Information. We have previously reported that a redox couple between dopamine and Au3+ in solution induces the seeded growth of small gold nanoparticles, and eventually into AuNS over time. Therefore, dopamine can simultaneously bind to the stent wire surface and capture Au3+ for the following AuNS growth. As shown in the SEM images (Figure 2c,d) of the AuNS-coated stent wire, a thin layer of AuNS was observed. Small gold nanoseeds were first grown on the wire surface, followed by the formation of complete gold nanoshell after 2 h of reaction using ethylene glycol as a reducing agent, as displayed in Figure 2e,f. Therefore, we can adjust the thickness of the AuNS by controlling the reaction time or amount of Au3+ added in the reaction (Figure S4). This synthesis method was easily extended to prepare AuNScoated stent under the same conditions. Eighteen stents were placed in a glass beaker containing pH 8.5 Tris buffer and dopamine. The color of all the stents changed from dark to brown, indicating successful formation of a PDA layer on the stent surface.29 The stent was washed with water and inserted into an ethylene glycol solution, followed by the addition of HAuCl4 into the solution. The reaction was carried out with stirring at 100 °C. After 2 h of reaction, the stent was removed and washed with water. As shown in Figure2g,h, compared to the stent with black color, the AuNS-coated stent has a light yellow color, which is the color of AuNS. This method is very
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RESULTS AND DISCUSSION Preparation of Gold Nanoshell-Coated Stents. To prepare AuNS-coated stent, a stent wire was used in the preliminary experiment. A thick layer of PDA was first grown onto the stent surface by immersing the stent wire into a solution of pH 8.5 Tris buffer containing dopamine.29 The color of the solution changed from bright yellow to dark brown over time, indicating the formation of PDA.30 In comparison 27525
DOI: 10.1021/acsami.6b09104 ACS Appl. Mater. Interfaces 2016, 8, 27523−27529
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increased only by ∼4 °C treated with an NIR laser at 0.5 W/ cm2. Thus, AuNS-coated stent exhibits a high photothermal effect and excellent stability, which is essential for in vivo PTT.31,32 In Vitro Photothermal Therapy Effect of Gold Nanoshell-Coated Stent. For biological applications, the ideal photothermal agents should be biocompatible, nontoxic, or low in toxicity.33 We evaluated the cytotoxicity of the modified stent using U87MG and OVCAR-8 cancer cells. After the stent wire was placed in cell culture medium for over 4 days, nearly no cell death was observed, which suggests that the stent is relatively nontoxic in vitro, as shown in Figure S2. Photothermal therapy efficacy of the gold nanoshell-coated stent was evaluated on U87MG cancer cells in vitro. The cancer cells were incubated with the functionalized stent wire in 24-well cell culture plate, and irradiated with an 808 nm laser at 0.25 W/cm2 for 3 min. As shown in Figure 4a−d, the cells treated with gold nanoshellcoated stent wire exhibited red color, indicating that the cells were dead. However, the cells away from the wire showed green color, and were not killed. Therefore, we can control the region of the photothermal heating by the irradiation time and laser power density, which is helpful for the future localized photothermal therapy. The cells treated with stent wire without gold nanoshell coating and laser irradiation were all alive, as shown in Figure 4 e−h, which suggested that the temperature surrounding the stent wire was not significantly increased. As shown in Figure 4i−l, nearly no cell death was found when U87MG cells were treated with gold nanoshell-coated stent wire but without laser irradiation. These results further confirmed that the gold nanoshell-coated stent can serve as an effective photothermal agent for cancer treatment.34,35 Application as Local Photothermal Therapy Agent. Considering the deep penetration using NIR light in biological tissues, AuNS-coated stents are susceptible to NIR light excitation.34 To investigate the photothermal effect of AuNScoated stent in tissues, first the AuNS-coated stent wire was placed on the surface of a piece of pork, followed by irradiation with laser as shown in Figure 5a. The temperature of the pork
simple and can be completed in a short time, providing the opportunity for large-scale synthesis of AuNS-coated stents. Because dopamine can be coated on most organic and inorganic materials owing to its mussel-inspired self-polymerized property, the PDA-induced formation of AuNS can be used to prepare different types of stents. Furthermore, PDA can be used as an absorbent for a series of metal ions. This can be used to synthesize various metal-coated stents such as copper sulfide, quantum dots, and iron oxide. Photothermal Effect of Gold Nanoshell-Coated Stent. Next, the photothermal effect of AuNS-coated stent irradiated with 808 nm NIR laser was investigated. Figure 3 showed that
Figure 3. Photothermal images (a) and temperature variation (b) of a stent coated with and without gold nanoshell irradiated with an 808 nm laser at 0.25 and 0.5 W/cm2, respectively.
the surface temperature of the stent rapidly reached ∼115 °C after being irradiated with laser at a power density of 0.5 W/ cm2 for 2 min. Even when the stent was treated with a laser at a lower power density of 0.25 W/cm2, the surface temperature of the stent still increased ∼80 °C after 2 min of irradiation. Benefiting from the stability of the AuNS, the temperature could be maintained above 110 °C for at least 40 min. This is useful for prolonged and continuous PTT. In contrast, the surface temperature of the stent without AuNS coating
Figure 4. Photographs and fluorescence images of U87MG cancer cells after photothermal therapy with AuNS-coated stent wire (a−d) and stent wire (e−h) irradiated by a laser (808 nm) at a power output of 0.25 W/cm2 for 3 min, and AuNS-coated stent wire without laser irradiation (i−l). Cells after irradiation and incubated for 12 h were stained with PI (dead, red) and calcein AM (live, green). 27526
DOI: 10.1021/acsami.6b09104 ACS Appl. Mater. Interfaces 2016, 8, 27523−27529
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Figure 5. Photographs (a, b) and temperature variation (c) of a pork treated with gold nanoshell-coated stent wire and NIR laser irradiation.
Figure 6. Photographs of the pig intestines implanted with gold nanoshell-coated stent (external surface: a−c; internal surface: d−f) before (a, d) and after (b, c, e, f) NIR laser irradiation at a power density of 0.25 W/cm2.
AuNS-coated stent was inserted into pig intestine to simulate a real esophageal environment. As shown in Figure 6a−c, an 808 nm laser (0.25 W/cm2) was used to irradiate the intestine with a laser spot size of 1 cm2. With increasing irradiation time, the temperature of the irradiated place increased and reached 70 °C in 3 min, thus burning the intestine. When the stent was removed, the inside face of the irradiated intestine was also found to be burned, indicating deep penetration by photothermal effect. Importantly, the irradiated area could be adjusted by the spot size of the laser spot (Figure 6d−f); this is helpful for the localized and accurate ablation of tumor in future applications. The same place of the intestine was irradiated with laser for five cycles; its temperature reached the same value, indicating the high stability of the stent. The temperature still increased to ∼70 °C when a stent implanted in intestine was immersed in PBS buffer and irradiated with 808 nm laser for 5 min (Figure S6). In cancer care, if an individual with a tumor that has not spread beyond the esophagus, doctors often recommend combining different types of treatment: radiation therapy, chemotherapy, and surgery. Such treatment causes many different side effects. For the AuNS-coated stent, it is able to use longer wavelength light (NIR laser), which is less energetic
was continuously monitored using an IR thermometer pre- and post-treatment. After irradiation with laser (0.25 W/cm2) for 2 min, the surface temperature was increased to ∼60 °C and the color of the irradiated area changed to white, indicating the high photothermal effect of the wire. At 24 h post-treatment, char formation was observed on the laser-treated area, further indicating a temperature increment. This corroborates with our previously reported PTT effect using gold nanoparticle vesicles. The pork treated with stent and laser irradiation did not show any observable temperature increase after 5 min of continuous laser irradiation. Next, the wire was inserted into the pork, as shown in Figure 5b. The pork around the wire changed to white, and its temperature reached ∼60 °C (Figure 5c). The depth of the white fat was about 2 cm in this experiment, indicating the deep penetration photothermal effect of the stent wire. More importantly, the therapy depth can be easily adjusted by the laser power density and irradiation time. In clinical applications, esophageal stents are usually used in the palliative treatment of advanced esophageal cancer. Besides the basic function of the stent, the AuNS-coated stent can also be used for localized PTT of tumors using NIR laser irradiation under the guidance of endoscopic examination. Thus, to further investigate the photothermal effect of the esophageal stent, 27527
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of this type of functionalized stent. Compared to bare metal stent, AuNS-modified stent will not only open the duct passageway but also suppress the tumor growth with high efficiency and accuracy in future clinical applications. The test and optimization of the laser power density, irradiation time, and evaluation of in vivo stability of the AuNS stent for cancer treatment are currently ongoing. We envision that the AuNScoated stent with these excellent merits enable their final applications in clinical esophageal cancer therapy.
and therefore less harmful to other cells and tissues than visible laser. AuNS-coated stent provides the possibility to exactly control the temperature increase in the tumor region by adjusting the laser power density, and also reduce the side effect to normal tissue. We have investigated the in vivo therapy potential of AuNS-coated stent. As shown in Figure 7a, two
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.6b09104. Photographs of a number of gold nanoshell-coated stent and in vitro cytotoxicity of gold nanoshell-coated stent (PDF)
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Author Contributions
All authors have given approval to the final version of the manuscript. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was supported by the Intramural Research Program of the National Institute of Biomedical Imaging and Bioengineering (NIBIB), National Institutes of Health (NIH).
Figure 7. Photographs (a) and tumor growth curves (b) of the control group and PTT therapy group of U87MG tumor mice before and at day 14 after laser irradiation. (circle: tumor; arrow: AuNS-coated stent wire).
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REFERENCES
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AuNS-coated stent wires were inserted into U87MG tumor (∼70 mm3). The whole tumor region was then irradiated with 808 nm laser at a power density at 0.25 W/cm2 for 5 min. The tumor growth in the AuNS-coated stent wire group was completely abrogated, in contrast to the continued growth of the tumors in the control group, as displayed in Figure 7a,b. For future clinical esophageal cancer therapy, this involves temporarily inserting an optical fiber into the esophagus using an endoscope, which can be used to guide the laser to treat exactly the tumor region without irradiation of normal tissue. We believe that PTT using AuNS-coated stent is a palliative or supportive care option to make swallowing easier and reduce the size of tumor efficiently, especially for those who choose not to or cannot have chemotherapy, radiation therapy, and surgery.
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CONCLUSIONS In summary, a novel photothermal AuNS-coated stent was prepared by using PDA as the Au3+ anchor. The thickness of the gold nanoshell was easily adjusted by the reaction time and amount of Au3+. The AuNS-coated stent showed a strong NIR light absorption and high photothermal effect, efficiently increasing the temperature of the pork and pig intestines irradiated with laser at a lower power density of laser for a short time. In vitro toxicity experiments showed excellent biocompatibility and biosafety of the AuNS-coated stent. The deep penetration of NIR laser and excellent stability of the AuNS coated-stent provide opportunities for true clinical applications 27528
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