Photoacoustic molecular imaging using combined acupuncture and gold nanorods as a composite contrast agent
Photoacoustic molecular imaging using combined acupuncture and gold nanorods as a composite contrast agent
In this study, we developed a novel photoacoustic imaging technique based on poly (ethyleneglycol)-coated (PEGylated) gold nanorods (PEG-GNRs) (as the contrast agent) combined with traditional Chinese medicine (TCM) acupuncture (as the auxiliary method) for quantitatively monitoring contrast enhancement in the vasculature of a mouse brain in vivo. This study takes advantage of the strong near-infrared absorption (peak at ~700 nm) of GNRs and the ability to adjust the hemodynamics of acupuncture. Experimental results show that photoacoustic tomography (PAT) successfully reveals the optical absorption variation of the vasculature of the mouse brain in response to intravenous administration of GNRs and acupuncture at the Zusanli acupoint (ST36) both individually and combined. The quantitative measurement of contrast enhancement indicates that the composite contrast agents (integration of acupuncture and GNRs) would greatly enhance the photoacoustic imaging contrast. The quantitative results also have the potential to estimate the local concentration of GNRs and even the real-time effects of acupuncture.
Xinxin Zhang：School of Electronic Science and Engineering, University of Electronic Science and Technology of China, Chengdu, Sichuan, P. R. ChinaCenter for Information in Biomedicine, University of Electronic Science and Technology of China, Sichuan, P. R. China
Jian Rong：Center for Information in Biomedicine, University of Electronic Science and Technology of China, Sichuan, P. R. ChinaSchool of Physics, University of Electronic Science and Technology of China, Chengdu, Sichuan, P. R. China
Huabei Jiang：School of Electronic Science and Engineering, University of Electronic Science and Technology of China, Chengdu, Sichuan, P. R. ChinaCenter for Information in Biomedicine, University of Electronic Science and Technology of China, Sichuan, P. R. ChinaDepartment of Medical Engineering, University of South Florida, Tampa, FL 33620, USA
【1】A. G. Bell, “On the production and reproduction of sound by light," Am. J. Sci. 20, 305–324 (1880).
【2】P. Beard, “Biomedical photoacoustic imaging," Interface Focus 1, 602–631 (2011).
【3】J. Tang, L. Xi, J. Zhou, H. Huang, T. Zhang, P. Carney, H. Jiang, “Noninvasive high-speed photoacoustic tomography of cerebral hemodynamicsin awake-moving rats," J. Cereb. Blood Flow Metab. 35, 1224–1232 (2015).
【4】D. Wu, L. Huang, M. S. Jiang, H. Jiang, “Contrast agents for photoacoustic and thermoacoustic imaging: A review," Int. J. Mol. Sci. 15, 23616–23639 (2014).
【5】A。 Taruttis, S。 Morscher, N。 C。 Burton, D。 Razansky, V。 Ntziachristos, “Fast multispectral optoacoustic tomography (MSOT) for dynamic imaging of pharmacokinetics and biodistribution in multiple organs," Plos One 7, e30491 (2012)。
【6】H。 Jiang, Photoacoustic Tomography, CRC Press (2014)。
【7】L。 Xi, S。 R。 Grobmyer, L。 Wu, R。 Chen, G。 Zhou, L。 G。 Gutwein, J。 Sun, W。 Liao, Q。 Zhou, H。 Xie, H。 Jiang, “Evaluation of breast tumor margins in vivo with intraoperative photoacoustic imaging," Opt。 Express 20, 8726–8731 (2012)。
【8】M。 Nasiriavanaki, J。 Xia, H。 Wan, A。 Q。 Bauer, J。 P。 Culver, L。 V。 Wang, “High-resolution photoacoustic tomography of resting-state functional connectivity in the mouse brain," Proc。 Natl。 Acad。 Sci。 111, 21 (2014)。
【9】D。 Wu, J。 Yang, G。 Zhang, H。 Jiang, “Noninvasive in vivo monitoring of collagenase induced intracerebral hemorrhage by photoacoustic tomography," Biomed。 Opt。 Exp。 8, 2276–2286 (2017)。
【10】D. Wu, X. Guo, R. Cui, M. Wu, Q. Shang, H. Jiang, “In vivo hemodynamic visualization of berberineinduced effect on the cerebral cortex of a mouse by photoacoustic tomography," Appl. Opt. 58, 1–8 (2019).
【11】P. Zhang, L. Li, L. Lin, P. Hu, J. Shi, Y. He, L. Zhu, Y. Zhou, L. V. Wang, “High resolution deep functional imaging of the whole mouse brain by photoacoustic computed tomography in vivo," J. Biophoton. 11, e201700024 (2018).
【12】S. Liu et al., “Electromagnetic–acoustic sensing for biomedical applications," Sensors 18(10), 3203 (2018).
【13】D. Wang, Y. Wu, J. Xia, “Review on photoacoustic imaging of the brain using nanoprobes," Neurophotonics 3(1), 010901 (2016).
【14】L。 Nie, Z。 Guo, L。 V。 Wang, “Photoacoustic tomography of monkey brain using virtual point ultrasonic transducers," J。 Biomed。 Opt。 16(7), 076005 (2011)。
【15】X. Wang, D. L. Chamberland, G. Xi, “Noninvasive reflection mode photoacoustic imaging through infant skull toward imaging of neonatal brains," J. Neurosci. Meth. 168(2), 412–421 (2008).
【16】X. Wang et al., “Reflection mode photoacoustic imaging through infant skull toward noninvasive imaging of neonatal brains," J. Neurosci. Meth. 168(2), 412–421 (2009).
【17】A. Hariri et al., “Functional photoacoustic tomography for neonatal brain imaging: Developments and challenges," Proc. Photons Plus Ultrasound: Imaging & Sensing. International Society for Optics and Photonics, p. 10642Z (2017).
【18】S。 Herrmann et al。, “Cerebral blood oxygenation measurements in neonates with optoacoustic technique," Soc。 Photo-Opt。 Instrum。 Eng。 (SPIE) Conf。 Series, p。 100640Q (2017)。
【19】C。 Huang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data," J。 Biomed。 Opt。 17(6), 066016 (2012)。
【20】A. R. Mohammadi-Nejad et al., “Neonatal brain resting-state functional connectivity imaging modalities," Photoacoustics S2213597917300368 (2018).
【21】K. Kim et al., “Photoacoustic imaging of early inflammatory response using gold nanorods," Appl. Phys. Lett. 90(22), 223901 (2007).
【22】H. W. Yang et al., “Magnetic gold-nanorod/PNIPAAmMA nanoparticles for dual magnetic resonance and photoacoustic imaging and targeted photothermal therapy," Biomaterials 34, 5651–5660 (2013).
【23】P。 H。 Wang et al。, “Gold-nanorod contrast-enhanced photoacoustic micro-imaging of focused-ultrasound induced blood-brain-barrier opening in a rat model," J。 Biomed。 Opt。 17(6), 061222 (2012)。
【24】P. C. Li et al., “In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods," Opt. Exp. 16, 18605–18615 (2008).
【25】J。 E。 Millstone et al。, “Observation of a quadrupole plasmon mode for a colloidal solution of gold nanoprisms," J。 Am。 Chem。 Soc。 127, 5312–5313 (2005)。
【26】P. K. Jain et al., “Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: Applications in biological imaging and biomedicine," J. Phys. Chem. B 110, 7238–7248 (2006).
【27】C。 M。 Chuang et al。, “Acupuncture stimulation at Baihui acupoint reduced cerebral infarct and increased dopamine levels in chronic cerebral hypoperfusion and ischemia-reperfusion injured Sprague-Dawley rats," Am。 J。 Chin。Med。 35(5), 779–791 (2007)。
【28】Y. F. Qian et al., “Effects of acupuncture at different acupoints on cerebral blood flow in cerebral ischemia model rats," Zhongguo Zhenjiu 29(3), 213–216 (2009).
【29】H。 Xu et al。, “Effects of acupuncture at Baihui (DU20) and Zusanli (ST36) on the expression of heat shock protein 70 and tumor necrosis factor α in the peripheral serum of cerebral ischemia-reperfusioninjured rats," Chin。 J。 Integr。 Med。 20(5), 369–374 (2014)。
【30】B. Zhu, Scientific Foundations of Acupuncture & Moxibustion, Qingdao Press (1998).
【31】B。 Z。 Chen et al。, “Photoacoustic imaging of cerebral hypoperfusion during acupuncture," Biomed。 Opt。 Exp。 6(9), 3225–3234 (2015)。
【32】T. Li et al., “Photoacoustic imaging of acupuncture effect in small animals," Biomed. Opt. Exp. 6(2), 433–442 (2015).
【33】J. Yang et al., “Photoacoustic microscopy of electronic acupuncture (EA) effect in small animals," J. Biophoton. 10(2), 217 (2016).
【34】W. Dan, H. Jiang, “Contrast enhanced photoacoustic tomograpgy of living mouse brain using combined acupuncture and contrast agents," Acta Laser Biol. Sin. 27(2), 133–141 (2018).
【35】G. Li et al., “Cortical activations upon stimulation of the sensorimotor-implicated acupoints," Magn. Reson. Imaging. 22(5), 639–644 (2004).
【36】D. Alimi, A. Geissmann, D. Gardeur, “Functional MRI of the human brain following auricular stimulation," Med. Acupuncture. 13(2), 64 (2009).
【37】C. M. Siedentopf et al., “Functional magnetic resonance imaging detects activation of the visual association cortex during laser acupuncture of the foot in humans," Neurosci. Lett. 327(1), 53–56 (2002).
【38】S。 S。 Yoo et al。, “Modulation of cerebellar activities by acupuncture stimulation: Evidence from fMRI study," Neuroimage 22(2), 932–940 (2004)。
【39】Z. H. Cho et al., “New findings of the correlation between acupoints and corresponding brain cortices using functional MRI," Proc. Natl. Acad. Sci. 95(5), 2670–2673 (1998).
【40】W. T. Zhang et al., “Evidence from brain imaging with fMRI supporting functional specificity of acupoints in humans," Neurosci. Lett. 354(1), 50–53 (2004).
【41】Y. Shifang, N. Mofan, W. Ling, “Hemodynamics effect of negative pressure on ischemic extremity," China J. Mod. Med. 11, 010 (2003).
【42】H. Maeda, H. Nakamura, J. Fang, “The EPR effect for macromolecular drug delivery to solid tumors: Improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo," Adv. Drug Deliv. Rev. 65(1), 71–79 (2013).
【43】H. Jiang et al., “Related method of selective opening blood brain barrier," Med. Recapitulate 11, 023 (2010).
【44】K。 Linnet, T。 B。 Ejsing, “A review on the impact of P-glycoprotein on the penetration of drugs into the brain。 Focus on psychotropic drugs," Eur。 Neuropsychopharmacol 18(3), 157–169 (2008)。
【45】M. A. Deli, “Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery," Biochim. Biophys. Acta 1788(4), 892–910 (2009).
【46】E。 Preston et al。, “Graded reversible opening of the rat blood-brain barrier by intracarotid infusion of sodium caprate," J。 Neurosci。 Meth。 168(2), 443–449 (2008)。
【47】R. Singh, J. W. Lillard Jr., “Nanoparticle-based targeted drug delivery," Exp. Mol. Pathol. 86(3), 215–223 (2009).
【48】L。 Liu et al。, “Biologically active core/shell nanoparticles self-assembled from cholesterol-terminated PEG-TAT for drug delivery across the blood-brain barrier," Biomaterials 29(10), 1509–1517 (2008)。
【49】F. Y. Yang, P. Y. Lee, “E±ciency of drug delivery enhanced by acoustic pressure during blood-brain barrier disruption induced by focused ultrasound," Int. J. Nanomed. 7, 2573–2582 (2012).
【50】Y。 C。 Kuo, C。 Y。 Kuo, “Electromagnetic interference in the permeability of saquinavir across the blood-brain barrier using nanoparticulate carriers," Int。 J。 Pharm。 351(1/2), 271–281 (2008)。
【51】Y。 Wu, G。 L。 Liu, “Radiotherpy-induced Bloodbrain Barrier disruption and its implication for chemotherapy," Chin。 J。 Neuro-Oncol。 5(1), 63–65 (2007)。
【52】K. P. Tan, X. M. Lin, “Research and development tendency on Blood-brain Barrier with Chinese Herbs and acupuncture," Chin. Arch. Traditional Chin. Med. 25(11), 2283–2285 (2007).
【53】J. Chen et al., “Gold nanocages: Bioconjugation and their potential use as optical imaging contrast agents," Nano Lett. 5(3), 473–477 (2005).
【54】W. C. W. Chan et al., “Luminescent quantum dots for multiplexed biological detection and imaging," Curr. Opin. Biotechnol. 13(1), 40–46 (2002).
【55】X. Gao et al., “In vivo molecular and cellular imaging with quantum dots," Curr. Opin. Biotechnol. 16(1), 63–72 (2005).
【56】X. Feng, F. Gao, Y. Zheng, “Thermally modulated photoacoustic imaging with super-paramagnetic iron oxide nanoparticles," Opt. Lett. 39(12), 3414–3417 (2014).
【57】Y. Jin et al., “Multifunctional nanoparticles as coupled contrast agents," Nat. Commun. 1, 41 (2010).
【58】A. De La Zerda et al., “Carbon nanotubes as photoacoustic molecular imaging agents in living mice," Nat. Nanotechnol. 3(9), 557–562 (2008).
【59】S。 Zanganeh et al。, “Photoacoustic imaging enhanced by indocyanine green-conjugated single-wall carbon nanotubes," J。 Biomed。 Opt。 18(9), 096006 (2013)。
【60】P。 K。 Avti et al。, “Detection, mapping, and quanti fication of single walled carbon nanotubes in histological specimens with photoacoustic microscopy," PLoS One 7(4), e35064 (2012)。
【61】V. P. Nguyen et al., “Enhancement of high-resolution photoacoustic imaging with indocyanine greenconjugated carbon nanotubes," Jpn. J. Appl. Phys. 54(7S1), 07HF04 (2015).
【62】S. K. Maji et al., “Upconversion nanoparticles as a contrast agent for photoacoustic imaging in live mice," Adv. Mater. 26(32), 5633–5638 (2014).
【63】J. Chen et al., “Gold nanocages: Engineering their structure for biomedical applications," Adv. Mater. 17(18), 2255–2261 (2005).
【64】Y。 Wang et al。, “Photoacoustic tomography of a nanoshell contrast agent in the in vivo rat brain," Nano Lett。 4(9), 1689–1692 (2004)。
【65】W. Lu et al., “Photoacoustic imaging of living mouse brain vasculature using hollow gold nanospheres," Biomaterials 31(9), 2617–2626 (2010).
【66】G. Xu et al., “Theranostic quantum dots for crossing blood-brain barrier in vitro and providing therapy of HIV-associated encephalopathy," Front. Pharmacol. 4, 1–8 (2013).
【67】S. Hanada et al., “Cell-based in vitro blood-brain barrier model can rapidly evaluate nanoparticles'' brain permeability in association with particle size and surface modification," Int. J. Mol. Sci. 15(2), 1812–1825 (2014).
【68】M. K. Garcia et al., “Systematic review of acupuncture in cancer care: A synthesis of the evidence," J. Clin. Oncol. 31(7), 952–960 (2013).
【69】J。 Liu et al。, “Probing low-copy-number proteins in a single living cell," Angewandte Chemie Int。 Ed。 55(42), 13215–13218 (2016)。
【70】W. Zhu, G. Xi, J. Ju, “Effect of acupuncture and Chinese medicine treatment on brain dopamine level of MPTP-lesioned C57BL mice," Acupuncture Res. 21(4), 46 (1996).
【71】J. Chen, “Influence of acupuncture on serum growth hormone level in patients with type II diabetes," Acupuncture Res. 26(4), 310–313 (2001).
【72】Y。 Shi et al。, “Effects of acupuncture combined with medicine on the expression of IFN-γ and IL-12 of colonic mucous membrane in ulcerative colitis rats," Acupuncture Res。 30(4), 215–218 (2005)。
【73】J. J. Cui et al., “Discussion on the novel clues for studying the underlying mechanisms of acupunctureinduced potentiation of the curative effect of medicines," Acupuncture Res. 35(2), 146–150 (2010).
【74】Y. Chen, W. Jia, Z. Cheng, “Effects of electroacupuncture on tropism of effective component of pubescent angelica root in the rat with adjuvant arthritis," Chin. Acupuncture Moxibust. 24(1), 59–61 (2004).
【75】Y. H. Gu, H. Z. Jin, S. D. Li, “The influence of acupuncture on the intracorporeal metabolism of tripterygium wilfordii in rate with adjuvant arthritis," Shanghai J. Acupuncture Moxibust. 20(5), 41–43 (2001).
【76】S. Zhang, H. Niu, “The effect of acupoint injection of capsaicin on the neurogenic inflammation induced by primary afferent reflexs," J. Xian Med. Univ. 21(1), 6–8 (2000).
【77】Z. Cheng, Y. Chen, L. Zhang, “Experimental study on effect of acupuncture on tropism of effective compositions of the Chinese drug in the rat," Chin. Acupuncture Moxibust. 22(1), 51–53 (2002).
【78】T. Zhang, C. Gao, Y. Guo, “Effects of moxibustion on the function ofMDR gene product, P-glycoprotein (P-170)," Acupuncture Res. 19(2), 69–71 (1994).
【79】E. Pinter, J. Szolcsanyi, “Plasma extravasation in the skin and pelvic organs evoked by antidromic stimulation of the lumbosacral dorsal roots of the rat," Neurosci. 68(2), 603–614 (1995).
【80】J。 Fang et al。, “Neurogenic inflammation evoked by stimulation of the acupoint through drr," J。 Xian Med。 Univ。 1999(2), 175 (1999)。
【81】D。 Cao, H。 Niu, Z。 Yan, “Neurogenic inflammation of the visceral organs evoked by electrical stimulation of acupoint in rats," Chin。 Acupuncture Moxibust。 21(11), 662–664 (2001)。
【82】S. Zhang, H. Niu, S. Jiang, “Nerogenic inflammation evoked by stimulation of acupoint through long axon reflex," J. Xian Med. Univ. 20(4), 438–440 (1999).
【83】X。 C。 Yu et al。, “Cross-talk between cardiac kappaopioid and beta-adrenergic receptors in developing hypertensive rats," J。 Mol。 Cell。 Cardiol。 31(3), 597 (1999)。
【84】J. Gao et al., “Acupuncture pretreatment protects heart from injury in rats with myocardial ischemia and reperfusion via inhibition of the β-adrenoceptor signaling pathway," Life Sci. 80(16), 1484–1489.
Dan Wu,Xinxin Zhang,Jian Rong,Huabei Jiang. Photoacoustic molecular imaging using combined acupuncture and gold nanorods as a composite contrast agent[J]. Journal of Innovative Optical Health Sciences, 2019, 12(3): 1941004
Dan Wu,Xinxin Zhang,Jian Rong,Huabei Jiang。 Photoacoustic molecular imaging using combined acupuncture and gold nanorods as a composite contrast agent[J]。 Journal of Innovative Optical Health Sciences, 2019, 12(3): 1941004