Development of wide-field high-resolution dual optical imaging platform for vasculature and morphological assessment of chronic kidney disease: A feasibility study

• Autorzy: Abu Saleah Sm , Lee Jaeyul , Seong Daewoon , Han Sangyeob , Park Kibeom , Hong Juyeon , Park Sooah , Kwon Yoon-Hee , Jung Woonggyu , Jeon Mansik , Kim Jeehyun

Identyfikatory

DOI

10.1016/j.bbe.2024.09.001

• Języki publikacji: EN

Abstrakty

EN

Chronic kidney disease (CKD) affects the morphological structure and causes significant degradation in kidney function, leading to renal replacement treatment in affected individuals. Vascular rarefaction is thought to be an important factor in accelerating kidney damage in CKD patients, therefore, the assessment of renal morphology and vasculature is crucial in nephrology. The objective of this study was to evaluate the morphological and vascular changes caused by CKD in mice kidneys. In this study, dual photoacoustic microscopy (PAM) and optical coherence microscopy (OCM) oriented wide-field high-resolution imaging modalities were employed for diseased renal imaging. The unilateral ureteral obstruction (UUO) model was used to prepare renal samples with CKD, and the developed wide-field dual imaging system was used to image both control and CKD-affected kidneys for assessing vascular and morphological changes during CKD progression. The obtained results reveal a gradual alteration in vascular intensity and pelvis space with the progress of UUO disease. Furthermore, a quantitative micro-vessel analysis was performed based on the node, junction, and mesh of the vessel, which provides details on the increasing microvascular-related characteristics in the peripheral area as the disease progresses. Thus, by concurrently employing the advantages of each optical imaging technique, the proposed method of assessing the OCM-based morphological and PAM-based vascular properties of the renal sample using a wide-field multimodal imaging system can be an efficient technique for whole volume analysis without any exogenous contrast agents in kidney histopathology.

Słowa kluczowe

EN

chronic kidney disease; optical coherence microscopy; photoacoustic microscopy; unilateral ureteral obstruction; disease model

PL

przewlekła choroba nerek; mikroskopia optyczna; mikroskopia fotoakustyczna; model choroby

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2024
• Tom: Vol. 44, no. 3
• Strony: 759--770
• Opis fizyczny: Bibliogr. 95 poz., rys., tab., wykr.

Twórcy

autor

Abu Saleah Sm

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

autor

Lee Jaeyul

• Division of Pulmonary and Critical Care Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA

autor

Seong Daewoon

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

autor

Han Sangyeob

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

autor

Park Kibeom

• Department of Biomedical Engineering, McKelvey School of Engineering, Washington University in St. Louis, St. Louis, MO 63130, USA
• Department of Biomedical Engineering, Ulsan National Institute of Science and Technology, 50 UNIST-gil, Ulsan 44919, Republic of Korea

autor

Hong Juyeon

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

autor

Park Sooah

• In Vivo Research Center, UNIST Central Research Facilities, Ulsan National Institute of Science and Technology (UNIST), Ulsan 44919, Republic of Korea

autor

Kwon Yoon-Hee

• In Vivo Research Center, UNIST Central Research Facilities, Ulsan National Institute of Science and Technology (UNIST), Ulsan 44919, Republic of Korea

autor

Jung Woonggyu

• Department of Biomedical Engineering, Ulsan National Institute of Science and Technology, 50 UNIST-gil, Ulsan 44919, Republic of Korea

autor

Jeon Mansik

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

autor

Kim Jeehyun

• School of Electronic and Electrical Engineering, College of IT Engineering, Kyungpook National University, 80, Daehak-ro, Buk-gu, Daegu 41566, Republic of Korea

Bibliografia

• [1] J.D. Kopple National kidney foundation K/DOQI clinical practice guidelines for nutrition in chronic renal failure Am J Kidney Dis, 37 (2001), pp. S66-S70.
• [2] K. Kalantar-Zadeh, T.H. Jafar, D. Nitsch, B.L. Neuen, V. Perkovic Chronic kidney disease The lancet, 398 (2021), pp. 786-802.
• [3] T.Y. Wong, J. Coresh, R. Klein, P. Muntner, D.J. Couper, A.R. Sharrett, et al. Retinal microvascular abnormalities and renal dysfunction: the atherosclerosis risk in communities study J Am Soc Nephrol, 15 (2004), pp. 2469-2476.
• [4] P. Kotlarsky, A. Bolotin, K. Dorfman, B. Knyazer, T. Lifshitz, J. Levy Link between retinopathy and nephropathy caused by complications of diabetes mellitus type 2 Int Ophthalmol, 35 (2015), pp. 59-66.
• [5] Ali BH, Adham SA, Al Za’abi M, Waly MI, Yasin J, Nemmar A, et al. Ameliorative effect of chrysin on adenine-induced chronic kidney disease in rats. PLoS One. 2015;10:e0125285.
• [6] Dong Z, Men J, Yang Z, Jerwick J, Li A, Tanzi RE, et al. FlyNet 2.0: drosophila heart 3D (2D+ time) segmentation in optical coherence microscopy images using a convolutional long short-term memory neural network. Biomedical Optics Express. 2020;11:1568-79.
• [7] D. Fliser Perspectives in renal disease progression: the endothelium as a treatment target in chronic kidney disease J Nephrol, 23 (2010), pp. 369-376.
• [8] Prasad N, Jha V. Hemodialysis in asia. Kidney Diseases. 2015;1:165-77.
• [9] A. Levey, R. Atkins, J. Coresh, E. Cohen, A. Collins, K.-U. Eckardt, et al. Chronic kidney disease as a global public health problem: approaches and initiatives – a position statement from kidney disease improving global outcomes Kidney Int, 72 (2007), pp. 247-259.
• [10] G.J. Schwartz, A. Munoz, M.F. Schneider, R.H. Mak, F. Kaskel, B.A. Warady, et al. New equations to estimate GFR in children with CKD J Am Soc Nephrol, 20 (2009), p. 629.
• [11] A.D. Rule, T.S. Larson, E.J. Bergstralh, J.M. Slezak, S.J. Jacobsen, F.G. Cosio Using serum creatinine to estimate glomerular filtration rate: accuracy in good health and in chronic kidney disease Ann Intern Med, 141 (2004), pp. 929-937.
• [12] M.-S. Wen, C.-Y. Wang, S.-L. Lin, K.-C. Hung Decrease in irisin in patients with chronic kidney disease PLoS One, 8 (2013), p. e64025.
• [13] Rahman T, Uddin MS. Speckle noise reduction and segmentation of kidney regions from ultrasound image. 2013 International Conference on Informatics, Electronics and Vision (ICIEV): IEEE; 2013. p. 1-5.
• [14] K. Scherer, E. Braig, K. Willer, M. Willner, A.A. Fingerle, M. Chabior, et al. Non-invasive differentiation of kidney stone types using X-ray dark-field radiography Sci Rep, 5 (2015), p. 9527.
• [15] G.R. Morrell, J.L. Zhang, V.S. Lee Magnetic resonance imaging of the fibrotic kidney J Am Soc Nephrol, 28 (2017), p. 2564.
• [16] H. Qiao, J. Bai, Y. Chen, J. Tian Kidney modelling for FDG excretion with PET Int J Biomed Imaging, 2007 (2007).
• [17] J. Missbach-Guentner, D. Pinkert-Leetsch, C. Dullin, R. Ufartes, D. Hornung, B. Tampe, et al. 3D virtual histology of murine kidneys-high resolution visualization of pathological alterations by micro computed tomography Sci Rep, 8 (2018), p. 1407.
• [18] G.K. Lui, A. Saidi, A.B. Bhatt, L.J. Burchill, J.F. Deen, M.G. Earing, et al. Diagnosis and management of noncardiac complications in adults with congenital heart disease: a scientific statement from the American Heart Association Circulation, 136 (2017), pp. e348-e392.
• [19] L. Yan, Y. Guo, J. Qi, Q. Zhu, L. Gu, C. Zheng, et al. Iodine and freeze-drying enhanced high-resolution MicroCT imaging for reconstructing 3D intraneural topography of human peripheral nerve fascicles J Neurosci Methods, 287 (2017), pp. 58-67.
• [20] G. Özkan, A. Kanli, N.M. Başeren, U. Arslan, İ. Tatar Validation of micro-computed tomography for occlusal caries detection: an in vitro study Braz Oral Res, 29 (2015), pp. 01-07.
• [21] J. Ehling, J. Bábíčková, F. Gremse, B.M. Klinkhammer, S. Baetke, R. Knuechel, et al. Quantitative micro-computed tomography imaging of vascular dysfunction in progressive kidney diseases J Am Soc Nephrol, 27 (2016), p. 520.
• [22] J. Foiret, H. Zhang, T. Ilovitsh, L. Mahakian, S. Tam, K.W. Ferrara Ultrasound localization microscopy to image and assess microvasculature in a rat kidney Sci Rep, 7 (2017), p. 13662.
• [23] M. Held, I. Santeramo, B. Wilm, P. Murray, R. Lévy Ex vivo live cell tracking in kidney organoids using light sheet fluorescence microscopy PLoS One, 13 (2018), p. e0199918.
• [24] G.C. Gobe, N.C. Bennett, M. West, P. Colditz, L. Brown, D.A. Vesey, et al. Increased progression to kidney fibrosis after erythropoietin is used as a treatment for acute kidney injury Am J Physiol-Renal Physiol, 306 (2014), pp. F681-F692.
• [25] R. Hlushchuk, C. Zubler, S. Barré, C. Correa Shokiche, L. Schaad, R. Röthlisberger, et al. Cutting-edge microangio-CT: new dimensions in vascular imaging and kidney morphometry Am J Physiol-Renal Physiol, 314 (2018), pp. F493-F499.
• [26] T.D. Hull, A. Agarwal, K. Hoyt New ultrasound techniques promise further advances in AKI and CKD J Am Soc Nephrol, 28 (2017), p. 3452.
• [27] S. Zhao, J. Hartanto, R. Joseph, C.-H. Wu, Y. Zhao, Y.-S. Chen Hybrid photoacoustic and fast super-resolution ultrasound imaging Nat Commun, 14 (2023), p. 2191.
• [28] W. Cao, S. Cui, L. Yang, C. Wu, J. Liu, F. Yang, et al. Contrast-enhanced ultrasound for assessing renal perfusion impairment and predicting acute kidney injury to chronic kidney disease progression Antioxid Redox Signal, 27 (2017), pp. 1397-1411.
• [29] S. Lei, G. Zhang, B. Zhu, X. Long, Z. Jiang, Y. Liu, et al. In vivo ultrasound localization microscopy imaging of the Kidney’s microvasculature with block-matching 3-D denoising IEEE Trans Ultrason Ferroelectr Freq Control, 69 (2021), pp. 523-533.
• [30] A. Klingberg, A. Hasenberg, I. Ludwig-Portugall, A. Medyukhina, L. Männ, A. Brenzel, et al. Fully automated evaluation of total glomerular number and capillary tuft size in nephritic kidneys using lightsheet microscopy J Am Soc Nephrol, 28 (2017), p. 452.
• [31] M. Jain, B.D. Robinson, B. Salamoon, O. Thouvenin, C. Boccara, S. Mukherjee Rapid evaluation of fresh ex vivo kidney tissue with full-field optical coherence tomography J Pathol Inform, 6 (2015), p. 53.
• [32] S. Faubel, N.U. Patel, M.E. Lockhart, M.A. Cadnapaphornchai Renal relevant radiology: use of ultrasonography in patients with AKI Clin J Am Soc Nephrol: CJASN, 9 (2014), p. 382.
• [33] C.-K. Peng, K.-L. Huang, C.-C. Lan, Y.-J. Hsu, G.-C. Wu, C.-H. Peng, et al. Experimental chronic kidney disease attenuates ischemia-reperfusion injury in an ex vivo rat lung model PLoS One, 12 (2017), p. e0171736.
• [34] Y. Wang, Y. Wang, G. Zheng, V. Lee, L. Ouyang, D. Chang, et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease Kidney Int, 72 (2007), pp. 290-299.
• [35] E.C. Jensen Types of imaging, Part 2: an overview of fluorescence microscopy Anat Rec Adv Integr Anat Evol Biol, 295 (2012), pp. 1621-1627.
• [36] E. Plotnikov, A. Kazachenko, M.Y. Vyssokikh, A. Vasileva, D. Tcvirkun, N. Isaev, et al. The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney Kidney Int, 72 (2007), pp. 1493-1502.
• [37] T. Morikawa, K. Takubo Use of imaging techniques to illuminate dynamics of hematopoietic stem cells and their niches Front Cell Dev Biol, 5 (2017), p. 62.
• [38] O. Gross, B. Beirowski, S.J. Harvey, C. McFadden, D. Chen, S. Tam, et al. DDR1-deficient mice show localized subepithelial GBM thickening with focal loss of slit diaphragms and proteinuria Kidney Int, 66 (2004), pp. 102-111.
• [39] S. Conti, N. Perico, R. Novelli, C. Carrara, A. Benigni, G. Remuzzi Early and late scanning electron microscopy findings in diabetic kidney disease Sci Rep, 8 (1) (2018), p. 4909.
• [40] Medina-Velo IA, Zuverza-Mena N, Tan W, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL. Biophysical methods of detection and quantification of uptake, translocation, and accumulation of nanoparticles. Plant Nanotechnology: Principles and Practices. 2016:29-63.
• [41] Dolezyczek H, Tamborski S, Majka P, Sampson D, Wojtkowski M, Wilczyński G, et al. In vivo brain imaging with multimodal optical coherence microscopy in a mouse model of thromboembolic photochemical stroke. Neurophotonics. 2020;7:015002.
• [42] Ascoli G, Bezhanskaya J, Tsytsarev V. Microscopy; 2014.
• [43] S.A. Saleah, D. Seong, R.E. Wijesinghe, S. Han, S. Kim, M. Jeon, et al. Development of a deviated focusing-based optical coherence microscope with a variable depth of focus for high-resolution imaging Opt Express, 31 (2023), pp. 1258-1268.
• [44] M.L. Onozato, P.M. Andrews, Q. Li, J. Jiang, A. Cable, Y. Chen Optical coherence tomography of human kidney J Urol, 183 (2010), pp. 2090-2094.
• [45] Hysi E, He X, Fadhel MN, Zhang T, Krizova A, Ordon M, et al. Photoacoustic imaging of kidney fibrosis for assessing pretransplant organ quality. JCI insight. 2020;5.
• [46] M. Mogensen, L. Thrane, T.M. Jørgensen, P.E. Andersen, G.B. Jemec OCT imaging of skin cancer and other dermatological diseases J Biophotonics, 2 (2009), pp. 442-451.
• [47] S.A. Saleah, P. Kim, D. Seong, R.E. Wijesinghe, M. Jeon, J. Kim A preliminary study of post-progressive nail-art effects on in vivo nail plate using optical coherence tomography-based intensity profiling assessment Sci Rep, 11 (2021), p. 666.
• [48] J. Lee, S.A. Saleah, B. Jeon, R.E. Wijesinghe, D.-E. Lee, M. Jeon, et al. Assessment of the inner surface roughness of 3D printed dental crowns via optical coherence tomography using a roughness quantification algorithm IEEE Access, 8 (2020), pp. 133854-133864.
• [49] Y. Shimada, A. Sadr, M.F. Burrow, J. Tagami, N. Ozawa, Y. Sumi Validation of swept-source optical coherence tomography (SS-OCT) for the diagnosis of occlusal caries J Dent, 38 (2010), pp. 655-665.
• [50] J. Lee, X. Du, J. Park, Q. Cui, R.R. Iyer, S.A. Boppart, et al. Tunable image-mapping optical coherence tomography Biomed Opt Express, 14 (2023), pp. 627-638.
• [51] J.P. Ehlers, J. Goshe, W.J. Dupps, P.K. Kaiser, R.P. Singh, R. Gans, et al. Determination of feasibility and utility of microscope-integrated optical coherence tomography during ophthalmic surgery: the DISCOVER Study RESCAN Results JAMA ophthalmology, 133 (2015), pp. 1124-1132.
• [52] Q. Li, M.L. Onozato, P.M. Andrews, C.-W. Chen, A. Paek, R. Naphas, et al. Automated quantification of microstructural dimensions of the human kidney using optical coherence tomography (OCT) Opt Express, 17 (2009), pp. 16000-16016.
• [53] Wang B, Wang H-W, Guo H, Anderson E, Tang Q, Wu T, et al. Optical coherence tomography and computer-aided diagnosis of a murine model of chronic kidney disease. J Biomed Opt. 2017;22:121706.
• [54] A.S. Levey, P.E. De Jong, J. Coresh, M. El Nahas, B.C. Astor, K. Matsushita, et al. The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report Kidney Int, 80 (2011), pp. 17-28.
• [55] S. Hu, L.V. Wang Photoacoustic imaging and characterization of the microvasculature J Biomed Opt, 15 (2010), pp. 011101-011115.
• [56] J.R. Montford, C. Bauer, E. Dobrinskikh, K. Hopp, M. Levi, M. Weiser-Evans, et al. Inhibition of 5-lipoxygenase decreases renal fibrosis and progression of chronic kidney disease Am J Physiol-Renal Physiol, 316 (2019), pp. F732-F742.
• [57] N. Sun, S. Zheng, D.L. Rosin, N. Poudel, J. Yao, H.M. Perry, et al. Development of a photoacoustic microscopy technique to assess peritubular capillary function and oxygen metabolism in the mouse kidney Kidney Int, 100 (2021), pp. 613-620.
• [58] E. Min, S. Ban, J. Lee, A. Vavilin, S. Baek, S. Jung, et al. Serial optical coherence microscopy for label-free volumetric histopathology Sci Rep, 10 (2020), p. 6711.
• [59] Q. Chen, J. Yu, B.M. Rush, S.D. Stocker, R.J. Tan, K. Kim Ultrasound super-resolution imaging provides a noninvasive assessment of renal microvasculature changes during mouse acute kidney injury Kidney Int, 98 (2020), pp. 355-365.
• [60] S. Ban, E. Min, S. Baek, H.M. Kwon, G. Popescu, W. Jung Optical properties of acute kidney injury measured by quantitative phase imaging Biomed Opt Express, 9 (2018), pp. 921-932.
• [61] D. Seong, S. Han, D. Jeon, Y. Kim, R.E. Wijesinghe, N.K. Ravichandran, et al. Dynamic compensation of path length difference in optical coherence tomography by an automatic temperature control system of optical fiber IEEE Access, 8 (2020), pp. 77501-77510.
• [62] Y. Kim, G.-I. Jung, D. Jeon, R.E. Wijesinghe, D. Seong, J. Lee, et al. Non-invasive optical coherence tomography data-based quantitative algorithm for the assessment of residual adhesive on bracket-removed dental surface Sensors, 21 (2021), p. 4670.
• [63] D. Seong, J. Kwon, D. Jeon, R.E. Wijesinghe, J. Lee, N.K. Ravichandran, et al. In situ characterization of micro-vibration in natural latex membrane resembling tympanic membrane functionally using optical doppler tomography Sensors, 20 (2019), p. 64.
• [64] D. Seong, W. Ki, P. Kim, J. Lee, S. Han, S. Yi, et al. Virtual intraoperative optical coherence tomography angiography integrated surgical microscope for simultaneous imaging of morphological structures and vascular maps in vivo Opt Lasers Eng, 151 (2022), Article 106943.
• [65] J. Lee, S. Han, D. Seong, J. Lee, S. Park, R.E. Wijesinghe, et al. Fully waterproof two-axis galvanometer scanner for enhanced wide-field optical-resolution photoacoustic microscopy Opt Lett, 45 (2020), pp. 865-868.
• [66] D. Seong, E. Lee, Y. Kim, S. Han, J. Lee, M. Jeon, et al. Three-dimensional reconstructing undersampled photoacoustic microscopy images using deep learning Photoacoustics, 29 (2023), Article 100429.
• [67] D. Seong, S. Yi, S. Han, J. Lee, S. Park, Y.-H. Hwang, et al. Target ischemic stroke model creation method using photoacoustic microscopy with simultaneous vessel monitoring and dynamic photothrombosis induction Photoacoustics, 27 (2022), Article 100376.
• [68] Seong D, Han S, Lee J, Lee E, Kim Y, Lee J, et al. Waterproof galvanometer scanner-based handheld photoacoustic microscopy probe for wide-field vasculature imaging in vivo. Photonics: MDPI; 2021. p. 305.
• [69] H. Kim, D. Seong, S. Han, H. Cho, J. Lee, R.E. Wijesinghe, et al. Whole-body imaging of Camponotus atrox using photoacoustic microscopy for three-dimensional morphological analysis: a preliminary study Opt Laser Technol, 167 (2023), Article 109754.
• [70] G. Carpentier, S. Berndt, S. Ferratge, W. Rasband, M. Cuendet, G. Uzan, et al. Angiogenesis analyzer for ImageJ - a comparative morphometric analysis of “endothelial tube formation assay” and “fibrin bead assay” Sci Rep, 10 (2020), p. 11568.
• [71] Manuelidis L. Prokaryotic SPHINX 1.8 REP protein is tissue‐specific and expressed in human germline cells. J Cellular Biochem. 2019;120:6198-208.
• [72] W. Kriz Structural organization of the renal medulla: comparative and functional aspects Am J Physiol-Regulat Integrative Comparative Physiology, 241 (1981), pp. R3-R16.
• [73] P. Stepka, M. Kratochvilova, M. Kuchynka, M. Raudenska, H.H. Polanska, T. Vicar, et al. Determination of renal distribution of zinc, copper, iron, and platinum in mouse kidney using LA-ICP-MS Biomed Res Int, 2021 (2021).
• [74] A. Narváez Barros, R. Guiteras, A. Sola, A. Manonelles, J. Morote, J.M. Cruzado Reversal unilateral ureteral obstruction: a mice experimental model Nephron, 142 (2019), pp. 125-134.
• [75] A. Babelova, D. Avaniadi, O. Jung, C. Fork, J. Beckmann, J. Kosowski, et al. Role of Nox4 in murine models of kidney disease Free Radic Biol Med, 53 (2012), pp. 842-853.
• [76] S. Gairola, C. Ram, A.M. Syed, P. Doye, U. Kulhari, M.N. Mugale, et al. Nootkatone confers antifibrotic effect by regulating the TGF-β/Smad signaling pathway in mouse model of unilateral ureteral obstruction Eur J Pharmacol, 910 (2021), Article 174479.
• [77] S. Klahr, J. Morrissey Obstructive nephropathy and renal fibrosis Am J Physiol-Renal Physiol, 283 (2002), pp. F861-F875.
• [78] G. Kökény, Á. Németh, J.B. Kopp, W. Chen, A.J. Oler, A. Manzéger, et al. Susceptibility to kidney fibrosis in mice is associated with early growth response-2 protein and tissue inhibitor of metalloproteinase-1 expression Kidney Int, 102 (2022), pp. 337-354.
• [79] N. Sakai, T. Wada, H. Yokoyama, M. Lipp, S. Ueha, K. Matsushima, et al. Secondary lymphoid tissue chemokine (SLC/CCL21)/CCR7 signaling regulates fibrocytes in renal fibrosis Proc Natl Acad Sci, 103 (2006), pp. 14098-14103.
• [80] B. Reich, K. Schmidbauer, M.R. Gomez, F.J. Hermann, N. Göbel, H. Brühl, et al. Fibrocytes develop outside the kidney but contribute to renal fibrosis in a mouse model Kidney Int, 84 (2013), pp. 78-89.
• [81] T.S. Puri, M.I. Shakaib, A. Chang, L. Mathew, O. Olayinka, A.W. Minto, et al. Chronic kidney disease induced in mice by reversible unilateral ureteral obstruction is dependent on genetic background Am J Physiol-Renal Physiol, 298 (2010), pp. F1024-F1032.
• [82] E. Seeliger, M. Sendeski, C.S. Rihal, P.B. Persson Contrast-induced kidney injury: mechanisms, risk factors, and prevention Eur Heart J, 33 (2012), pp. 2007-2015.
• [83] M.M. Sendeski Pathophysiology of renal tissue damage by iodinated contrast media Clin Exp Pharmacol Physiol, 38 (2011).
• [84] G.L. Bakris, N.A. Lass, D. Glock Renal hemodynamics in radiocontrast medium-induced renal dysfunction: a role for dopamine-1 receptors Kidney Int, 56 (1999), pp. 206-210.
• [85] S.N. Heyman, J. Reichman, M. Brezis Pathophysiology of radiocontrast nephropathy: a role for medullary hypoxia Invest Radiol, 34 (1999), p. 685.
• [86] M. Brezis, S. Rosen Hypoxia of the renal medulla - its implications for disease N Engl J Med, 332 (1995), pp. 647-655.
• [87] A. Boscheri, C. Weinbrenner, B. Botzek, K. Reynen, E. Kuhlisch, R. Strasser Failure of ascorbic acid to prevent contrast-media induced nephropathy in patients with renal dysfunction Clin Nephrol, 68 (2007), pp. 279-286.
• [88] H.-C. Lee, S.-H. Sheu, I.-H. Liu, C.-C. Lee, C.-C. Hsieh, H.-W. Yen, et al. Impact of short-duration administration of N-acetylcysteine, probucol and ascorbic acid on contrast-induced cytotoxicity J Nephrol, 25 (2012), p. 56.
• [89] L. Zhou, H. Chen Prevention of contrast-induced nephropathy with ascorbic acid Intern Med, 51 (2012), pp. 531-535.
• [90] M.J. Goolsby National kidney foundation guidelines for chronic kidney disease: evaluation, classification, and stratification J Am Acad Nurse Pract, 14 (2002), pp. 238-242.
• [91] L.A. Stevens, J. Coresh, T. Greene, A.S. Levey Assessing kidney function - measured and estimated glomerular filtration rate N Engl J Med, 354 (2006), pp. 2473-2483.
• [92] J. Zhang, D. Peng, W. Qin, W. Qi, X. Liu, Y. Luo, et al. Organ-PAM: photoacoustic microscopy of whole-organ multiset vessel systems Laser Photonics Rev, 17 (2023), p. 2201031.
• [93] G. Huang, J. Lv, Y. He, J. Yang, L. Zeng, L. Nie In vivo quantitative photoacoustic evaluation of the liver and kidney pathology in tyrosinemia Photoacoustics, 28 (2022), Article 100410.
• [94] C.A. Goebel, E. Brown, F.B. Fahlbusch, A.L. Wagner, A. Buehler, T. Raupach, et al. High-resolution label-free mapping of murine kidney vasculature by raster-scanning optoacoustic mesoscopy: an ex vivo study Mol Cell Pediatr, 9 (2022), p. 13.
• [95] O. Ogunlade, J.J. Connell, J.L. Huang, E. Zhang, M.F. Lythgoe, D.A. Long, et al. In vivo three-dimensional photoacoustic imaging of the renal vasculature in preclinical rodent models Am J Physiol-Renal Physiol, 314 (2018), pp. F1145-F1153.

Uwagi

Opracowanie rekordu ze środków MNiSW, umowa nr POPUL/SP/0154/2024/02 w ramach programu "Społeczna odpowiedzialność nauki II" - moduł: Popularyzacja nauki (2025).