CODA: quantitative 3D reconstruction of large tissues at cellular resolution
Open accessPublished version of a preprint
Abstract
A central challenge in biology is obtaining high-content, high-resolution information while analyzing tissue samples at volumes relevant to disease progression. We address this here with CODA, a method to reconstruct exceptionally large (up to multicentimeter cubed) tissues at subcellular resolution using serially sectioned hematoxylin and eosin-stained tissue sections. Here we demonstrate CODA's ability to reconstruct three-dimensional (3D) distinct microanatomical structures in pancreas, skin, lung and liver tissues. CODA allows creation of readily quantifiable tissue volumes amenable to biological research. As a testbed, we assess the microanatomy of the human pancreas during tumorigenesis within the branching pancreatic ductal system, labeling ten distinct structures to examine heterogeneity and structural transformation during neoplastic progression. We show that pancreatic precancerous lesions develop into distinct 3D morphological phenotypes and that pancreatic cancer tends to spread far from the bulk tumor along collagen fibers that are highly aligned to the 3D curves of ductal, lobular, vascular and neural structures. Thus, CODA establishes a means to transform broadly the structural study of human diseases through exploration of exhaustively labeled 3D microarchitecture.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
3D image processing is adopted to construct microanatomical structures of skin.
“Three-dimensional image processing is also adopted to construct microanatomical structures of skin [59]”
From Artificial Intelligence in the Histopathological Assessment of Non-Neoplastic Skin Disorders: A Narrative Review with Future Perspectives (2025) · cites this paper as [59]
In PDAC patient tissue, multiplexed myeloid, lymphoid, and functional antibody panels mapped the spatial relationship between myeloid and T cell populations.
“Illustrating the utility of this approach, multiplexed myeloid, lymphoid, and functional antibody panels were able to spatially define the relationship between myeloid and T cell populations in PDAC patient tissue275.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [275]
Although immune infiltration and behavior varied among patients, spatial analysis revealed extensive heterogeneity within individual patients.
“Of note, while many differences in immune infiltration and behavior were found between different patients, this ability to spatially assess these data allowed the observation of widespread heterogeneity in individual patients.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [275]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Siegel, R. L., Miller, K. D., & Jemal, A. (2020) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21590 · Cited by 20,444 · see citing works
Encoder-Decoder with Atrous Separable Convolution for Semantic Image Segmentation
Chen, L.-C., Zhu, Y., Papandreou, G., Schroff, F., & Adam, H. (2018) · Lecture Notes in Computer Science · doi:10.1007/978-3-030-01234-2_49 · Cited by 20,054 · see citing works
Siegel, R. L., Miller, K. D., Fuchs, H. E., & Jemal, A. (2021) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21654 · Cited by 16,522 · see citing works
QuPath: Open source software for digital pathology image analysis
Bankhead, P., Loughrey, M. B., Fernández, J. A., Dombrowski, Y., McArt, D. G., Dunne, P. D., McQuaid, S., Gray, R. T., Murray, L. J., Coleman, H. G., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17204-5 · Cited by 8,908 · see citing works
Coudray, N., Ocampo, P. S., Sakellaropoulos, T., Narula, N., Snuderl, M., Fenyö, D., Moreira, A. L., Razavian, N., & Tsirigos, A. (2018) · Nature Medicine · doi:10.1038/s41591-018-0177-5 · Cited by 2,930 · see citing works
Structural and molecular interrogation of intact biological systems
Chung, K., Wallace, J., Kim, S.-Y., Kalyanasundaram, S., Andalman, A. S., Davidson, T. J., Mirzabekov, J. J., Zalocusky, K. A., Mattis, J., Denisin, A. K., et al. (2013) · Nature · doi:10.1038/nature12107 · Cited by 2,008 · see citing works
Drost, J., & Clevers, H. (2018) · Nature Reviews Cancer · doi:10.1038/s41568-018-0007-6 · Cited by 1,790 · see citing works
Hover-Net: Simultaneous segmentation and classification of nuclei in multi-tissue histology images
Graham, S., Vu, Q. D., Raza, S. E. A., Azam, A. S., Tsang, Y. W., Kwak, J. T., & Rajpoot, N. (2019) · Medical Image Analysis · doi:10.1016/j.media.2019.101563 · Cited by 1,445 · see citing works
Lehmann, B. D., Jovanović, B., Chen, X., Estrada, M. V., Johnson, K. N., Shyr, Y., Moses, H. L., Sanders, M. E., & Pietenpol, J. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157368 · Cited by 1,435 · see citing works
Liebig, C., Ayala, G., Wilks, J. A., Berger, D. H., & Albo, D. (2009) · Cancer · doi:10.1002/cncr.24396 · Cited by 1,243 · see citing works
Richardson, D. S., & Lichtman, J. W. (2015) · Cell · doi:10.1016/j.cell.2015.06.067 · Cited by 1,095 · see citing works
Hruban, R. H., Takaori, K., Klimstra, D. S., Adsay, N. V., Albores-Saavedra, J., Biankin, A. V., Biankin, S. A., Compton, C., Fukushima, N., Furukawa, T., et al. (2004) · American Journal of Surgical Pathology · doi:10.1097/01.pas.0000126675.59108.80 · Cited by 1,091 · see citing works
Self-citationSaltz, J., Gupta, R., Hou, L., Kurc, T., Singh, P., Nguyen, V., Samaras, D., Shroyer, K. R., Zhao, T., Batiste, R., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.086 · Cited by 1,027 · see citing works
Single-Cell Phenotyping within Transparent Intact Tissue through Whole-Body Clearing
Yang, B., Treweek, J. B., Kulkarni, R. P., Deverman, B. E., Chen, C., Lubeck, E., Shah, S., Cai, L., & Gradinaru, V. (2014) · Cell · doi:10.1016/j.cell.2014.07.017 · Cited by 933 · see citing works
Basturk, O., Hong, S.-M., Wood, L. D., Adsay, N. V., Albores-Saavedra, J., Biankin, A. V., Brosens, L. A. A., Fukushima, N., Goggins, M., Hruban, R. H., et al. (2015) · American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000533 · Cited by 864 · see citing works
Self-citationEarly Detection of Pancreatic Cancer: Opportunities and Challenges
Singhi, A. D., Koay, E. J., Chari, S. T., & Maitra, A. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.01.259 · Cited by 841 · see citing works
Huang, L., Holtzinger, A., Jagan, I., BeGora, M. D., Lohse, I., Ngai, N., Nostro, M. C., Wang, R., Muthuswamy, L. B., Crawford, H. C., et al. (2015) · Nature Medicine · doi:10.1038/nm.3973 · Cited by 745 · see citing works
The role of collagen in cancer: from bench to bedside
Xu, S., Xu, H., Wang, W., Li, S., Li, H., Li, T., Zhang, W., Yu, X., & Liu, L. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-2058-1 · Cited by 735 · see citing works
Physical Activity, Obesity, Height, and the Risk of Pancreatic Cancer
Michaud, D. S. (2001) · JAMA · doi:10.1001/jama.286.8.921 · Cited by 663 · see citing works
The anatomy and physiology of nerve injury
Sunderland, S. S. (1990) · Muscle & Nerve · doi:10.1002/mus.880130903 · Cited by 551 · see citing works
OpenSlide: A vendor-neutral software foundation for digital pathology
Goode, A., Gilbert, B., Harkes, J., Jukic, D., & Satyanarayanan, M. (2013) · Journal of Pathology Informatics · doi:10.4103/2153-3539.119005 · Cited by 546 · see citing works
Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study
Canto, M. I., Goggins, M., Hruban, R. H., Petersen, G. M., Giardiello, F. M., Yeo, C., Fishman, E. K., Brune, K., Axilbund, J., Griffin, C., et al. (2006) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2006.02.005 · Cited by 524 · see citing works
Self-citationMorris, J. P., Cano, D., Sekine, S., Wang, S. C., & Hebrok, M. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40045 · Cited by 391 · see citing works
(2006) · PubMed · Cited by 347 · see citing works
Self-citationWalker, R. A. (2006) · Histopathology · doi:10.1111/j.1365-2559.2006.02514.x · Cited by 319 · see citing works
Chiang, S., Cabrera, R. M., & Segall, J. E. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00238.2015 · Cited by 310 · see citing works
Cellular and Molecular Probing of Intact Human Organs
Zhao, S., Todorov, M. I., Cai, R., -Maskari, R. A., Steinke, H., Kemter, E., Mai, H., Rong, Z., Warmer, M., Stanic, K., et al. (2020) · Cell · doi:10.1016/j.cell.2020.01.030 · Cited by 292 · see citing works
Murakami, T. C., Mano, T., Saikawa, S., Horiguchi, S. A., Shigeta, D., Baba, K., Sekiya, H., Shimizu, Y., Tanaka, K. F., Kiyonari, H., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0109-1 · Cited by 290 · see citing works
Susaki, E. A., Shimizu, C., Kuno, A., Tainaka, K., Li, X., Nishi, K., Morishima, K., Ono, H., Ode, K. L., Saeki, Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15906-5 · Cited by 286 · see citing works
Update on pancreatic intraepithelial neoplasia.
Hruban, R. H., Maitra, A., & Goggins, M. (2008) · PubMed Central · Cited by 245 · see citing works
Self-citationFraley, S. I., Wu, P.-H., He, L., Feng, Y., Krishnamurthy, R., Longmore, G. D., & Wirtz, D. (2015) · Scientific Reports · doi:10.1038/srep14580 · Cited by 234 · see citing works
Self-citationKuett, L., Catena, R., Özcan, A., Plüss, A., Ali, H. R., Sa’d, M. A., Alon, S., Aparicio, S. A. J. R., Battistoni, G., Balasubramanian, S., et al. (2021) · Nature Cancer · doi:10.1038/s43018-021-00301-w · Cited by 219 · see citing works
Drifka, C. R., Loeffler, A. G., Mathewson, K., Keikhosravi, A., Eickhoff, J. C., Liu, Y., Weber, S. M., Kao, W. J., & Eliceiri, K. W. (2016) · Oncotarget · doi:10.18632/oncotarget.12772 · Cited by 216 · see citing works
Acinar Cells Contribute to the Molecular Heterogeneity of Pancreatic Intraepithelial Neoplasia
Zhu, L., Shi, G., Schmidt, C. M., Hruban, R. H., & Konieczny, S. F. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.061176 · Cited by 213 · see citing works
Self-citationMeta-analysis of recurrence pattern after resection for pancreatic cancer
Tanaka, M., Mihaljević, A. L., Probst, P., Heckler, M., Klaiber, U., Heger, U., Büchler, M. W., & Hackert, T. (2019) · British journal of surgery · doi:10.1002/bjs.11295 · Cited by 202 · see citing works
ANATOMY, FUNCTION, AND PATHOPHYSIOLOGY OF PERIPHERAL NERVES AND NERVE COMPRESSION
Lundborg, G., & Dahlin, L. B. (1996) · Hand Clinics · doi:10.1016/s0749-0712(21)00303-6 · Cited by 199 · see citing works
Taniuchi, K., Nakagawa, H., Hosokawa, M., Nakamura, T., Eguchi, H., Ohigashi, H., Ishikawa, O., Katagiri, T., & Nakamura, Y. (2005) · Cancer Research · doi:10.1158/0008.5472.can-04-3646 · Cited by 190 · see citing works
Tissue curvature and apicobasal mechanical tension imbalance instruct cancer morphogenesis
Messal, H. A., Alt, S., Ferreira, R. M. M., Gribben, C., Wang, V. M.-Y., Cotoi, C. G., Salbreux, G., & Behrens, A. (2019) · Nature · doi:10.1038/s41586-019-0891-2 · Cited by 180 · see citing works
Rios, A. C., Capaldo, B. D., Vaillant, F., Pal, B., van Ineveld, R. L., Dawson, C. A., Chen, Y., Nolan, E., Fu, N. Y., Jackling, F. C., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.02.010 · Cited by 170 · see citing works
Djuric, U., Zadeh, G. M., Aldape, K., & Diamandis, P. (2017) · npj Precision Oncology · doi:10.1038/s41698-017-0022-1 · Cited by 169 · see citing works
Cuccarese, M. F., Dubach, J. M., Pfirschke, C., Engblom, C., Garris, C. S., Miller, M. A., Pittet, M., & Weissleder, R. (2017) · Nature Communications · doi:10.1038/ncomms14293 · Cited by 167 · see citing works
Plentz, R. R., Park, J., Rhim, A. D., Abravanel, D. L., Hezel, A. F., Sharma, S. V., Gurumurthy, S., Deshpande, V., Kenific, C. M., Settleman, J. E., et al. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.01.008 · Cited by 162 · see citing works
Harnessing non-destructive 3D pathology
Liu, J. T. C., Glaser, A. K., Bera, K., True, L. D., Reder, N. P., Eliceiri, K. W., & Madabhushi, A. (2021) · Nature Biomedical Engineering · doi:10.1038/s41551-020-00681-x · Cited by 158 · see citing works
Toward Routine Use of 3D Histopathology as a Research Tool
Roberts, N. P., Magee, D. R., Song, Y., Brabazon, K. J., Shires, M., Crellin, D., Orsi, N. M., Quirke, R., Quirke, P., & Treanor, D. E. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.01.033 · Cited by 153 · see citing works
HistoSegNet: Semantic Segmentation of Histological Tissue Type in Whole Slide Images
Chan, L., Hosseini, M. S., Rowsell, C. H., Plataniotis, K. N., & Damaskinos, S. (2019) · IEEE/CVF International Conference on Computer Vision (ICCV) · doi:10.1109/iccv.2019.01076 · Cited by 152 · see citing works
Drifka, C. R., Tod, J., Loeffler, A. G., Liu, Y., Thomas, G. J., Eliceiri, K. W., & Kao, W. J. (2015) · Modern Pathology · doi:10.1038/modpathol.2015.97 · Cited by 138 · see citing works
Nirschl, J., Janowczyk, A. R., Peyster, E. G., Frank, R., Margulies, K. B., Feldman, M. D., & Madabhushi, A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0192726 · Cited by 130 · see citing works
Why is pancreatic cancer so deadly? The pathologist's view
Hruban, R. H., Gaida, M. M., Thompson, E., Hong, S., Noë, M., Brosens, L. A., Jongepier, M., Offerhaus, G. J. A., & Wood, L. D. (2019) · The Journal of Pathology · doi:10.1002/path.5260 · Cited by 115 · see citing works
Self-citationXie, W., Reder, N. P., Koyuncu, C., Leo, P., Hawley, S. J., Huang, H., Mao, C., Postupna, N. O., Kang, S., Serafin, R., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-2843 · Cited by 108 · see citing works
3D reconstruction of multiple stained histology images
Song, Y., Treanor, D. E., Bulpitt, A. J., & Magee, D. R. (2013) · Journal of Pathology Informatics · doi:10.4103/2153-3539.109864 · Cited by 88 · see citing works
Detection of pancreatic cancer tumours and precursor lesions by cathepsin E activity in mouse models
Cruz‐Monserrate, Z., Abd‐Elgaliel, W. R., Grote, T., Deng, D., Ji, B., Arumugam, T., Wang, H., Tung, C., & Logsdon, C. D. (2011) · Gut · doi:10.1136/gutjnl-2011-300544 · Cited by 74 · see citing works
Puls, T. J., Tan, X., Whittington, C. F., & Voytik‐Harbin, S. L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188870 · Cited by 73 · see citing works
Histological 3D reconstruction and in vivo lineage tracing of the human endometrium
Tempest, N., Jansen, M., Baker, A., Hill, C. J., Hale, M., Magee, D. R., Treanor, D. E., Wright, N. A., & Hapangama, D. K. (2020) · The Journal of Pathology · doi:10.1002/path.5478 · Cited by 70 · see citing works
Axer, H., Axer, M., Krings, T., & Keyserlingk, D. G. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(00)00349-6 · Cited by 66 · see citing works
Hong, S., JUNG, D., Kiemen, A. L., Gaida, M. M., Yoshizawa, T., Braxton, A. M., Noë, M., Lionheart, G., Oshima, K., Thompson, E. D., et al. (2019) · Modern Pathology · doi:10.1038/s41379-019-0409-3 · Cited by 62 · see citing works
Self-citationHigh-throughput ballistic injection nanorheology to measure cell mechanics
Wu, P.-H., Hale, C. M., Chen, W.-C., Lee, J. S. H., Tseng, Y., & Wirtz, D. (2012) · Nature Protocols · doi:10.1038/nprot.2011.436 · Cited by 55 · see citing works
Self-citationComparative analysis of tissue reconstruction algorithms for 3D histology
Kartasalo, K., Latonen, L., Vihinen, J., Visakorpi, T., Nykter, M., & Ruusuvuori, P. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty210 · Cited by 51 · see citing works
Cancerization of the Pancreatic Ducts
Hutchings, D., Waters, K. M., Weiss, M. J., Wolfgang, C. L., Makary, M. A., He, J. P., Cameron, J. L., Wood, L. D., & Hruban, R. H. (2018) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000001148 · Cited by 47 · see citing works
Self-citationZhang, J.-F., Hua, R., Sun, Y.-W., Liu, W. C., Huo, Y.-M., Liu, D.-J., & Li, J. (2013) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2013.14.9.5133 · Cited by 45 · see citing works
A qualitative comparison of ten tissue clearing techniques.
Orlich, M. M., & Kiefer, F. (2018) · PubMed · doi:10.14670/hh-11-903 · Cited by 43 · see citing works
Histopathology in 3D: From three-dimensional reconstruction to multi-stain and multi-modal analysis
Magee, D. R., Song, Y., Gilbert, S., Roberts, N. P., Wijayathunga, N., Wilcox, R. K., Bulpitt, A. J., & Treanor, D. E. (2015) · Journal of Pathology Informatics · doi:10.4103/2153-3539.151890 · Cited by 42 · see citing works
Three‐dimensional analysis of extrahepatic cholangiocarcinoma and tumor budding
Yoshizawa, T., Hong, S., JUNG, D., Noë, M., Kiemen, A. L., Wu, P., Wirtz, D., Hruban, R. H., Wood, L. D., & Oshima, K. (2020) · The Journal of Pathology · doi:10.1002/path.5474 · Cited by 37 · see citing works
Self-citationAntibody stabilization for thermally accelerated deep immunostaining
Lai, H. M., Tang, Y., Lau, Z. Y. H., Campbell, R. A. A., Yau, J. C. N., Chan, C. C. Y., Chan, D. C. W., Wong, T. Y., Wong, H. K. T., Yan, L. Y. C., et al. (2022) · Nature Methods · doi:10.1038/s41592-022-01569-1 · Cited by 37 · see citing works
Integration of 3D multimodal imaging data of a head and neck cancer and advanced feature recognition
Lotz, J. M., Hoffmann, F. S., Lotz, J., Heldmann, S., Trede, D., Oetjen, J., Becker, M. S., Ernst, G., Maaß, P., Alexandrov, T., et al. (2016) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2016.08.018 · Cited by 31 · see citing works
Mesoscopic 3D imaging of pancreatic cancer and Langerhans islets based on tissue autofluorescence
Hahn, M., Nord, C., Franklin, O., Alanentalo, T., Isaksson‐Mettävainio, M., Morini, F., Eriksson, M., Korsgren, O., Sund, M., & Ahlgren, U. (2020) · Scientific Reports · doi:10.1038/s41598-020-74616-6 · Cited by 21 · see citing works
Characterization of tumor‐associated macrophages in prostate cancer transgenic mouse models
de Groot, A. E., Myers, K. V., Krueger, T. E. G., Kiemen, A. L., Nagy, N. H., Brame, A., Torres, V. E., Zhang, Z., Trabzonlu, L., Brennen, W. N., et al. (2021) · The Prostate · doi:10.1002/pros.24139 · Cited by 20 · see citing works
Self-citationZooming in: high resolution 3D reconstruction of differently stained histological whole slide images
Lotz, J., Berger, J., Müller, B., Breuhahn, K., Grabe, N., Heldmann, S., Homeyer, A., Lahrmann, B., Laue, H., Olesch, J., et al. (2014) · Proceedings of SPIE, the International Society for Optical Engineering/Proceedings of SPIE · doi:10.1117/12.2043381 · Cited by 15 · see citing works
VISTA: VIsual Semantic Tissue Analysis for pancreatic disease quantification in murine cohorts
Ternes, L., Huang, G., Lanciault, C., Thibault, G., Riggers, R. R., Gray, J. W., Muschler, J. L., & Chang, Y. H. (2020) · Scientific Reports · doi:10.1038/s41598-020-78061-3 · Cited by 8 · see citing works
Huang, L., Holtzinger, A., Jagan, I., Nostro, M. C., Wang, R., Muthuswamy, L. B., Arrowsmith, C. H., Cleary, S. P., Schaeffer, D., Roehrl, M. H. A., et al. (2016) · Cancer Research · doi:10.1158/1538-7445.panca16-b45 · Cited by 5 · see citing works
Jaffe, J. S., Waddingham, W., Barmpoutis, P., & Jansen, M. (2021) · doi:10.1136/gutjnl-2020-bsgcampus.36 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- [2]Kartasalo K. Comparative analysis of tissue reconstruction algorithms for 3D histology. Bioinformatics 34, 3013 (2018). 29684099 PMC6129300
- [3]Wu PH High-throughput ballistic injection nanorheology to measure cell mechanics. Nat. Protoc. 2012 71 7, 155– 170 (2012). PMC4332792 22222790
- [4]Graham S. Hover-Net: Simultaneous segmentation and classification of nuclei in multi-tissue histology images. Med. Image Anal. 58, 101563 (2019). 31561183
- [5]Bankhead P. QuPath: Open source software for digital pathology image analysis. Sci. Reports 2017 71 7, 1– 7 (2017). PMC5715110 29203879
- [7]Fraley SI Three-dimensional matrix fiber alignment modulates cell migration and MT1-MMP utility by spatially and temporally directing protrusions. Sci. Reports 2015 51 5, 1– 13 (2015). PMC4589685 26423227
Cited by
Sorted by citations
Pancreatic cancer: Advances and challenges
Halbrook, C. J., Lyssiotis, C. A., Pasca di Magliano, M., & Maitra, A. (2023) · Cell · doi:10.1016/j.cell.2023.02.014 · Cited by 1,321 · see citing works
Greenwald, N. F., Miller, G., Moen, E., Kong, A., Kagel, A., Dougherty, T., Fullaway, C. C., McIntosh, B. J., Leow, K. X., Schwartz, M. S., et al. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-01094-0 · Cited by 953 · see citing works
Spatial omics and multiplexed imaging to explore cancer biology
Lewis, S. M., Asselin-Labat, M.-L., Nguyen, Q. H., Berthelet, J., Tan, X., Wimmer, V. C., Mérino, D., Rogers, K. L., & Naik, S. H. (2021) · Nature Methods · doi:10.1038/s41592-021-01203-6 · Cited by 609 · see citing works
Embracing cancer complexity: Hallmarks of systemic disease
Swanton, C., Bernard, E., Abbosh, C., André, F., Auwerx, J. H., Balmain, A., Bar‐Sagi, D., Bernards, R., Bullman, S., DeGregori, J. V., et al. (2024) · Cell · doi:10.1016/j.cell.2024.02.009 · Cited by 555 · see citing works
Stoop, T. F., Javed, A. A., Oba, A., Koerkamp, B. G., Seufferlein, T. T. W., Wilmink, J. W., & Besselink, M. G. (2025) · The Lancet · doi:10.1016/s0140-6736(25)00261-2 · Cited by 552 · see citing works
Artificial intelligence for digital and computational pathology
Song, A. H., Jaume, G., Williamson, D. F. K., Lu, M. Y., Vaidya, A., Miller, T. R., & Mahmood, F. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-023-00096-8 · Cited by 356 · see citing works
Spatial components of molecular tissue biology
Palla, G., Fischer, D. S., Regev, A., & Theis, F. J. (2022) · Nature Biotechnology · doi:10.1038/s41587-021-01182-1 · Cited by 315 · see citing works
Unbiased spatial proteomics with single-cell resolution in tissues
Mund, A., Brunner, A.-D., & Mann, M. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.05.022 · Cited by 259 · see citing works
Advances in spatial transcriptomic data analysisPreprint
Dries, R., Chen, J. G., Rossi, N. D., Khan, M. M., Sistig, A., & Yuan, G. (2021) · Genome Research · doi:10.1101/gr.275224.121 · Cited by 236 · see citing works
Cancer associated fibroblasts in cancer development and therapy
Jia, H., Chen, X., Zhang, L., & Chen, M. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-025-01688-0 · Cited by 252 · see citing works
Spatiotemporal omics for biology and medicine
Liu, L., Chen, A., Li, Y., Mulder, J., Heyn, H., & Xu, X. (2024) · Cell · doi:10.1016/j.cell.2024.07.040 · Cited by 239 · see citing works
Miller, B. F., Huang, F., Atta, L., Sahoo, A., & Fan, J. (2022) · Nature Communications · doi:10.1038/s41467-022-30033-z · Cited by 208 · see citing works
Spatial biology of cancer evolution
Seferbekova, Z., Lomakin, A., Yates, L. R., & Gerstung, M. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00553-x · Cited by 210 · see citing works
Advances in molecular pathology and therapy of non-small cell lung cancer
Huang, Q., Li, Y., Huang, Y., Wu, J., Bao, W., Xue, C., Li, X., Dong, S., Dong, Z., & Hu, S. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02243-6 · Cited by 197 · see citing works
Decoding the tumor microenvironment with spatial technologies
Walsh, L. A., & Quail, D. F. (2023) · Nature Immunology · doi:10.1038/s41590-023-01678-9 · Cited by 191 · see citing works
Harnessing non-destructive 3D pathology
Liu, J. T. C., Glaser, A. K., Bera, K., True, L. D., Reder, N. P., Eliceiri, K. W., & Madabhushi, A. (2021) · Nature Biomedical Engineering · doi:10.1038/s41551-020-00681-x · Cited by 158 · see citing works
3D genomic mapping reveals multifocality of human pancreatic precancers
Braxton, A. M., Kiemen, A. L., Grahn, M. P., Forjaz, A., Parksong, J., Babu, J. M., Lai, J., Zheng, L., Niknafs, N., Jiang, L., et al. (2024) · Nature · doi:10.1038/s41586-024-07359-3 · Cited by 158 · see citing works
Self-citationSTalign: Alignment of spatial transcriptomics data using diffeomorphic metric mapping
Clifton, K., Anant, M. M.-G., Aihara, G., Atta, L., Aimiuwu, O. K., Kebschull, J. M., Miller, M. I., Tward, D. J., & Fan, J. (2023) · Nature Communications · doi:10.1038/s41467-023-43915-7 · Cited by 139 · see citing works
Spatial landscapes of cancers: insights and opportunities
Chen, J., Larsson, L., Swarbrick, A., & Lundeberg, J. (2024) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-024-00926-7 · Cited by 153 · see citing works
Spatial mapping of cellular senescence: emerging challenges and opportunities
Gurkar, A. U., Gerencser, A. A., Mora, A. L., Nelson, A. C., Zhang, A. R., Lagnado, A. B., Enninful, A., Benz, C., Furman, D., Beaulieu, D., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00446-6 · Cited by 139 · see citing works
Self-citationLiu, Y., Dai, Y., & Wang, L. (2025) · Cancer Cell · doi:10.1016/j.ccell.2025.12.009 · Cited by 146 · see citing works
Research on Artificial-Intelligence-Assisted Medicine: A Survey on Medical Artificial Intelligence
Gou, F., Liu, J., Xiao, C., & Wu, J. (2024) · Diagnostics · doi:10.3390/diagnostics14141472 · Cited by 128 · see citing works
Unsupervised discovery of tissue architecture in multiplexed imaging
Kim, J., Rustam, S., Mosquera, J. M., Randell, S. H., Shaykhiev, R., Rendeiro, A. F., & Elemento, O. (2022) · Nature Methods · doi:10.1038/s41592-022-01657-2 · Cited by 111 · see citing works
Xie, W., Reder, N. P., Koyuncu, C., Leo, P., Hawley, S. J., Huang, H., Mao, C., Postupna, N. O., Kang, S., Serafin, R., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-2843 · Cited by 108 · see citing works
Analysis of 3D pathology samples using weakly supervised AI
Song, A. H., Williams, M., Williamson, D. F. K., Chow, S. S. L., Jaume, G., Gao, G., Zhang, A., Chen, B., Baras, A. S., Serafin, R. J., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.035 · Cited by 108 · see citing works
AI-driven 3D bioprinting for regenerative medicine: From bench to bedside
Zhang, Z., Zhou, X., Fang, Y., Xiong, Z., & Zhang, T. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.11.021 · Cited by 121 · see citing works
Virtual alignment of pathology image series for multi-gigapixel whole slide images
Gatenbee, C., Baker, A., Prabhakaran, S., Swinyard, O., Slebos, R. J. C., Mandal, G., Mulholland, E. J., Andor, N., Marusyk, A., Leedham, S. J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40218-9 · Cited by 98 · see citing works
PanIN and CAF transitions in pancreatic carcinogenesis revealed with spatial data integration
Bell, A. T. F., Mitchell, J. T., Kiemen, A. L., Lyman, M. R., Fujikura, K., Lee, J. W., Coyne, E. M., Shin, S. M., Nagaraj, S., Deshpande, A. M., et al. (2024) · Cell Systems · doi:10.1016/j.cels.2024.07.001 · Cited by 70 · see citing works
Self-citationJohnson, J., Bergman, D. R., da Rocha, H. L., Zhou, D. L., Cramer, E. M., McLean, I. C., Dance, Y. W., Booth, M. I., Nicholas, Z., Lopez-Vidal, T. Y., et al. (2025) · Cell · doi:10.1016/j.cell.2025.06.048 · Cited by 68 · see citing works
Self-citationThe tumour microenvironment in pancreatic cancer — new clinical challenges, but more opportunities
Kung, H., Zheng, K., Zimmerman, J. W., & Zheng, L. (2025) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-025-01077-z · Cited by 69 · see citing works
Fischman, S., Pérez‐Ánker, J., Tognetti, L., Naro, A. D., Suppa, M., Cinotti, É., Viel, T., Monnier, J., Rubegni, P., del Mármol, V., et al. (2022) · Scientific Reports · doi:10.1038/s41598-021-04395-1 · Cited by 63 · see citing works
Probing the physical hallmarks of cancer
Nia, H. T., Munn, L. L., & Jain, R. K. (2025) · Nature Methods · doi:10.1038/s41592-024-02564-4 · Cited by 51 · see citing works
Artificial intelligence and digital pathology: clinical promise and deployment considerations
Zarella, M. D., McClintock, D. S., Batra, H. V., Gullapalli, R. R., Valante, M., Tan, V. O., Dayal, S., Oh, K. S., Lara, H., Garcia, C., et al. (2023) · Journal of medical imaging · doi:10.1117/1.jmi.10.5.051802 · Cited by 49 · see citing works
Infrared spectroscopic laser scanning confocal microscopy for whole-slide chemical imaging
Yeh, K. L., Sharma, I., Falahkheirkhah, K., Confer, M. P., Orr, A. C., Liu, Y., Phal, Y. D., Ho, R.-J., Mehta, M., Bhargava, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40740-w · Cited by 48 · see citing works
A comprehensive review of spatial transcriptomics data alignment and integration
Khan, M. A., Arslanturk, S., & Drăghici, S. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf536 · Cited by 55 · see citing works
Montagud, A., Ponce-de-León, M., & Valencia, A. (2021) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2021.100385 · Cited by 46 · see citing works
Spatial multiplexing and omics
Carstens, J. L., Krishnan, S., Rao, A. U. K., Sorace, A. G., Seeley, E. H., Borgogno, S. F., & Burks, J. K. (2024) · Nature Reviews Methods Primers · doi:10.1038/s43586-024-00330-6 · Cited by 49 · see citing works
Zhao, C., Xu, Z., Wang, X., Tao, S., MacDonald, W. A., He, K., Poholek, A. C., Chen, K., Huang, H., & Chen, W. (2024) · Briefings in Bioinformatics · doi:10.1093/bib/bbae052 · Cited by 43 · see citing works
Pancreatic Cancer Detection using Machine and Deep Learning Techniques
Gupta, A., Koul, A., & Kumar, Y. (2022) · International Conference on Innovative Practices in Technology and Management (ICIPTM) · doi:10.1109/iciptm54933.2022.9754010 · Cited by 42 · see citing works
Kiemen, A. L., Damanakis, A. I., Braxton, A. M., He, J. P., Laheru, D. A., Fishman, E. K., Chames, P., Almagro-Pérez, C., Wu, P., Wirtz, D., et al. (2023) · Med · doi:10.1016/j.medj.2022.11.009 · Cited by 42 · see citing works
Self-citationDeshpande, A. M., Loth, M., Sidiropoulos, D. N., Zhang, S., Yuan, L., Bell, A. T. F., Zhu, Q., Ho, W. J., Santa-Maria, C. A., Gilkes, D. M., et al. (2023) · Cell Systems · doi:10.1016/j.cels.2023.03.004 · Cited by 41 · see citing works
Self-citationGiotto Suite: a multiscale and technology-agnostic spatial multiomics analysis ecosystem
Chen, J. G., Chávez, J., O’Brien, M., Xu, J., Ruiz, E. C., Wang, W., Amin, I., Sheridan, J. P., Shin, S. C., Hasyagar, S. V., et al. (2025) · Nature Methods · doi:10.1038/s41592-025-02817-w · Cited by 63 · see citing works
Mi, H., Sivagnanam, S., Ho, W. J., Zhang, S., Bergman, D. R., Deshpande, A. M., Baras, A. S., Jaffee, E. M., Coussens, L. M., Fertig, E. J., et al. (2024) · Briefings in Bioinformatics · doi:10.1093/bib/bbae421 · Cited by 38 · see citing works
Mechanical tension mobilizes Lgr6 + epidermal stem cells to drive skin growth
Xue, Y., Lyu, C., Taylor, A. L., van Ee, A., Kiemen, A. L., Choi, Y. G., Khavanian, N., Henn, D., Lee, C., Hwang, L., et al. (2022) · Science Advances · doi:10.1126/sciadv.abl8698 · Cited by 36 · see citing works
Self-citationDefining and modeling dynamic spatial heterogeneity within tumor microenvironments
Bareham, B. R., Dibble, M., & Parsons, M. (2024) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2024.102422 · Cited by 37 · see citing works
Vanea, C., Džigurski, J., Rukins, V., Dodi, O., Siigur, S., Salumäe, L., Meir, K. S., Parks, W. T., Hochner‐Celnikier, D., Fraser, A., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46986-2 · Cited by 36 · see citing works
Park, J., Shin, S., Kim, G., Cho, H., Ryu, D., Ahn, D., Heo, J. E., Clemenceau, J. R. V., Barnfather, I., Kim, M., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59820-0 · Cited by 36 · see citing works
Spatial landmark detection and tissue registration with deep learning
Ekvall, M., Bergenstråhle, L., Andersson, A., Czarnewski, P., Olegård, J., Käll, L., & Lundeberg, J. (2024) · Nature Methods · doi:10.1038/s41592-024-02199-5 · Cited by 35 · see citing works
Pentimalli, T. M., Schallenberg, S., León-Periñán, D., Legnini, I., Theurillat, I., Thomas, G., Boltengagen, A., Fritzsche, S., Nimo, J., Ruff, L., et al. (2025) · Cell Systems · doi:10.1016/j.cels.2025.101261 · Cited by 34 · see citing works
Liu, J. T. C., Glaser, A. K., Poudel, C., & Vaughan, J. C. (2023) · Annual Review of Analytical Chemistry · doi:10.1146/annurev-anchem-091222-092734 · Cited by 31 · see citing works
Perspective on quantitative phase imaging to improve precision cancer medicine
Liu, Y., & Uttam, S. (2024) · Journal of Biomedical Optics · doi:10.1117/1.jbo.29.s2.s22705 · Cited by 30 · see citing works
Forjaz, A., Vaz, E., Matos-Romero, V., Joshi, S., Queiroga, V., Braxton, A. M., Jiang, A. C., Fujikura, K., Cornish, T. C., Hong, S., et al. (2025) · Cell Reports Methods · doi:10.1016/j.crmeth.2025.101075 · Cited by 30 · see citing works
Self-citationJanssen, B. V., Theijse, R. T., van Roessel, S. R., de Ruiter, R., Berkel, A., Huiskens, J., Busch, O. R., Wilmink, J. W., Geert Kazemier, M., Valkema, P., et al. (2021) · Cancers · doi:10.3390/cancers13205089 · Cited by 30 · see citing works
Hui-lin, Y., Karl, M. N., Wang, W., Starich, B., Tan, H., Kiemen, A. L., Pucsek, A. B., Kuo, Y., Russo, G. C., Pan, T., et al. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.07.008 · Cited by 29 · see citing works
Self-citationDeep learning identification of stiffness markers in breast cancer
Sneider, A., Kiemen, A. L., Kim, J. H., Wu, P.-H., Habibi, M., White, M. J., Phillip, J., Gu, L., & Wirtz, D. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121540 · Cited by 17 · see citing works
Self-citationGhose, S., Ju, Y., McDonough, E., Ho, J., Karunamurthy, A. D., Chadwick, C. M., Cho, S., Rose, R., Corwin, A. D., Surrette, C., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04991-z · Cited by 27 · see citing works
Crawford, A. J., Forjaz, A., Bons, J., Bhorkar, I., Roy, T., Schell, D., Queiroga, V., Ren, K., Kramer, D., Huang, W., et al. (2024) · Science Advances · doi:10.1126/sciadv.adp6285 · Cited by 26 · see citing works
Self-citationWang, R., Hastings, W. J., Saliba, J. G., Bao, D., Huang, Y., Maity, S., Ahmad, O. M. K., Hu, L., Wang, S., Fan, J., et al. (2024) · ACS Nano · doi:10.1021/acsnano.4c11505 · Cited by 26 · see citing works
Timakova, A., Ananev, V. V., Fayzullin, A. L., Makarov, V. V., Иванова, Е., Shekhter, A. B., & Timashev, P. S. (2023) · Biomolecules · doi:10.3390/biom13091327 · Cited by 24 · see citing works
Mathur, S., Chen, S., & Rejniak, K. A. (2024) · npj Systems Biology and Applications · doi:10.1038/s41540-023-00327-z · Cited by 23 · see citing works
Joshi, S., Forjaz, A., Han, K. S., Shen, Y., Queiroga, V., Selaru, F. A., Gérard, M., Xenes, D., Matelsky, J., Wester, B. A., et al. (2025) · Nature Methods · doi:10.1038/s41592-025-02712-4 · Cited by 22 · see citing works
Self-citationRuusuvuori, P., Valkonen, M., Kartasalo, K., Valkonen, M., Visakorpi, T., Nykter, M., & Latonen, L. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e08762 · Cited by 21 · see citing works
Giotto Suite: a multi-scale and technology-agnostic spatial multi-omics analysis ecosystemPreprint
Chen, J. G., Chávez, J., O’Brien, M., Xu, J., Ruiz, E. C., Wang, W., Amin, I., Sarfraz, I., Guckhool, P., Sistig, A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.26.568752 · Cited by 21 · see citing works
Levy, J. J., Davis, M. J., Chacko, R. S., Davis, M. J., Fu, L. J., Goel, T., Pamal, A., Nafi, I., Angirekula, A., Suvarna, A., et al. (2024) · npj Precision Oncology · doi:10.1038/s41698-023-00477-7 · Cited by 20 · see citing works
Engineering the future of 3D pathology
Liu, J. T. C., Chow, S. S. L., Colling, R. T., Downes, M. R., Farré, X., Humphrey, P. A., Janowczyk, A. R., Mirtti, T. K., Verrill, C. L., Zlobec, I., et al. (2023) · The Journal of Pathology Clinical Research · doi:10.1002/cjp2.347 · Cited by 20 · see citing works
Comparison of consecutive and restained sections for image registration in histopathology
Lotz, J., Weiss, N., van der Laak, J. A. W. M., & Heldmann, S. (2023) · Journal of medical imaging · doi:10.1117/1.jmi.10.6.067501 · Cited by 20 · see citing works
FEM based simulation of magnetic drug targeting in a multibranched vessel model
Lindemann, M. C., Luttke, T., Nottrodt, N., Schmitz‐Rode, T., & Slabu, I. (2021) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2021.106354 · Cited by 19 · see citing works
The 3D Revolution in Cancer Discovery
Wang, L., Li, M., & Hwang, T. H. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-23-1499 · Cited by 19 · see citing works
Revolutionizing cancer research with spatial proteomics and visual intelligence
Quail, D. F., & Walsh, L. A. (2024) · Nature Methods · doi:10.1038/s41592-024-02542-w · Cited by 19 · see citing works
Advances in bioengineering pancreatic tumor-stroma physiomimetic Biomodels
Monteiro, M. V., Ferreira, L. P., Rocha, M., Gaspar, V. M., & Mano, J. F. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121653 · Cited by 19 · see citing works
Kiemen, A. L., Dbouk, M. H., Diwan, E. A., Forjaz, A., Dequiedt, L., Baghdadi, A., Madani, S. P., Grahn, M. P., Jones, C. K., Vedula, S. S., et al. (2024) · Pancreas · doi:10.1097/mpa.0000000000002288 · Cited by 18 · see citing works
Self-citationMultiomics Empowers Predictive Pancreatic Cancer Immunotherapy
Montagne, J. M., Jaffee, E. M., & Fertig, E. J. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200660 · Cited by 18 · see citing works
PanIN or IPMN? Redefining Lesion Size in 3 Dimensions
Kiemen, A. L., Dequiedt, L., Shen, Y., Zhu, Y., Matos-Romero, V., Forjaz, A., Campbell, K., Dhana, W., Cornish, T. C., Braxton, A. M., et al. (2024) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000002245 · Cited by 18 · see citing works
Self-citationThyroid cancer under the scope of emerging technologies
Tarabichi, M., Demetter, P., Craciun, L., Maenhaut, C., & Detours, V. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111491 · Cited by 18 · see citing works
OʼBrien, J., Niehaus, P., Chang, K., Remark, J., Barrett, J., Dasgupta, A., Adenegan, M., Salimian, M., Kevas, Y., Chandrasekaran, K., et al. (2024) · Brain · doi:10.1093/brain/awae100 · Cited by 17 · see citing works
Self-citationImage analyses for engineering advanced tissue biomanufacturing processes
Allenby, M. C., & Woodruff, M. A. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121514 · Cited by 17 · see citing works
Lyman, M. R., Mitchell, J. T., Raghavan, S., Kagohara, L. T., Huff, A. L., Haldar, S. D., Shin, S. M., Guinn, S. R., Barrett, B., Longway, G., et al. (2025) · JCI Insight · doi:10.1172/jci.insight.191595 · Cited by 16 · see citing works
Self-citationSidiropoulos, D. N., Shin, S. M., Wetzel, M., Girgis, A. A., Bergman, D. R., Danilova, L., Perikala, S., Shu, D. H., Montagne, J. M., Deshpande, A. M., et al. (2025) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-25-0387 · Cited by 16 · see citing works
Self-citationCadavid, J. L., Latour, S., Nowlan, F., Co, I. L., Landon‐Brace, N., Wouters, B. G., Grünwald, B. T., Nitz, M., Jackson, H. W., & McGuigan, A. P. (2022) · Advanced Healthcare Materials · doi:10.1002/adhm.202201846 · Cited by 16 · see citing works
Pinkert‐Leetsch, D., Frohn, J., Ströbel, P., Alves, F., Salditt, T., & Missbach‐Guentner, J. (2023) · Cancer Imaging · doi:10.1186/s40644-023-00559-6 · Cited by 16 · see citing works
Fayzullin, A. L., Иванова, Е., Grinin, V., Ermilov, D., Solovyeva, S. E., Balyasin, M. V., Bakulina, A., Nikitin, P. V., Valieva, Y., Kalinichenko, A. M., et al. (2024) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2024.08.011 · Cited by 16 · see citing works
Intraparenchymal metastases as a cause for local recurrence of pancreatic cancer
Kiemen, A. L., Choi, Y. G., Braxton, A. M., Almagro-Pérez, C., Graham, S., Grahn, M. P., Nanda, N., Roberts, N. J., Wood, L. D., Wu, P., et al. (2022) · Histopathology · doi:10.1111/his.14839 · Cited by 15 · see citing works
Self-citationMiller, B. F., Huang, F., Atta, L., Sahoo, A., & Fan, J. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.15.448381 · Cited by 15 · see citing works
Advancing Cardiovascular Research With Single-Cell and Spatial Transcriptomics
Li, K., Samiei, S., Pikulska, D., Foecking, S., & Kuppe, C. (2026) · Circulation Research · doi:10.1161/circresaha.125.325795 · Cited by 15 · see citing works
Lapierre-Landry, M., Liu, Y., Bayat, M., Wilson, D. L., & Jenkins, M. W. (2023) · Biomedical Optics Express · doi:10.1364/boe.480230 · Cited by 13 · see citing works
Doyle, J., Green, B., Eminizer, M., Jiménez‐Sánchez, D., Lu, S., Engle, E. L., Xu, H., Ogurtsova, A., Lai, J., Soto-Diaz, S., et al. (2023) · Laboratory Investigation · doi:10.1016/j.labinv.2023.100175 · Cited by 14 · see citing works
Blueprints from plane to space: outlook of next‐generation three‐dimensional histopathology
Yoshikawa, A. L., Omura, T., Takahashi‐Kanemitsu, A., & Susaki, E. A. (2024) · Cancer Science · doi:10.1111/cas.16095 · Cited by 13 · see citing works
Ngo, T. B., DeStefano, S., Liu, J., Su, Y. P., Shroff, H., Vishwasrao, H. D., & Sadtler, K. (2023) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.37515 · Cited by 13 · see citing works
High‐Resolution 3D Printing of Pancreatic Ductal Microanatomy Enabled by Serial Histology
Kiemen, A. L., Forjaz, A., Sousa, R., Han, K. S., Hruban, R. H., Wood, L. D., Wu, P., & Wirtz, D. (2024) · Advanced Materials Technologies · doi:10.1002/admt.202301837 · Cited by 13 · see citing works
Self-citationTen challenges and opportunities in computational immuno-oncology
Bao, R., Hutson, A. D., Madabhushi, A., Jönsson, V. D., Rosario, S. R., Barnholtz‐Sloan, J. S., Fertig, E. J., Marathe, H. G., Harris, L. N., Altreuter, J., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-009721 · Cited by 13 · see citing works
High-resolution molecular atlas of a lung tumor in 3DPreprint
Pentimalli, T. M., Schallenberg, S., León-Periñán, D., Legnini, I., Theurillat, I., Thomas, G., Boltengagen, A., Fritzsche, S., Nimo, J., Ruff, L., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.10.539644 · Cited by 13 · see citing works
Highly Multiplexed 3D Profiling of Cell States and Immune Niches in Human TumoursPreprint
Yapp, C., Nirmal, A. J., Zhou, F., Wong, A. Y. H., Tefft, J. B., Lu, Y. D., Shang, Z., Maliga, Z., Llopis, P. D. L. M. M., Murphy, G. F., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.10.566670 · Cited by 13 · see citing works
Iyer, M. K., Fletcher, A. A., Okoye, J. O., Shi, C., Chen, F., Kanu, E. N., Eckhoff, A. M., Bao, M., di Magliano, M. P., Frankel, T. L., et al. (2025) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-1529 · Cited by 12 · see citing works
The New Era of Three-Dimensional Histoarchitecture of the Human Endometrium
Yamaguchi, M., Yoshihara, K., Yachida, N., Suda, K., Tamura, R., Ishiguro, T., & Enomoto, T. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11080713 · Cited by 12 · see citing works
Deciphering cell-fate trajectories using spatiotemporal single-cell transcriptomic data
Zhang, Z., Wang, Z., Sun, Y., Shen, J., Peng, Q., Li, T., & Zhou, P. (2025) · npj Systems Biology and Applications · doi:10.1038/s41540-025-00624-9 · Cited by 12 · see citing works
Wang, B., Zou, L., Chen, J., Cao, Y., Cai, Z., Qiu, Y., Mao, L., Wang, Z.-Q., Chen, J., Gui, L., et al. (2023) · IEEE Journal of Biomedical and Health Informatics · doi:10.1109/jbhi.2023.3340686 · Cited by 11 · see citing works
Three-dimensional model of normal human dermal tissue using serial tissue sections
Liu, P., Zhang, T., & Huang, Y. (2024) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2024.1347159 · Cited by 11 · see citing works
Aspects and outcomes of surveillance for individuals at high-risk of pancreatic cancer
Bogdanski, A. M., van Hooft, J. E., Boekestijn, B., Bonsing, B. A., Wasser, M. N. J. M., Klatte, D. C. F., & van Leerdam, M. E. (2024) · Familial Cancer · doi:10.1007/s10689-024-00368-1 · Cited by 12 · see citing works
Burlingame, E. A., Ternes, L., Lin, J., Chen, Y.-A., Kim, E. N., Gray, J. W., Santagata, S., Sorger, P. K., & Chang, Y. H. (2023) · Frontiers in Bioinformatics · doi:10.3389/fbinf.2023.1275402 · Cited by 10 · see citing works
Karageorgos, G. M., Cho, S., McDonough, E. M., Chadwick, C. M., Ghose, S., Owens, J. R., Jung, K. J., Machiraju, R., West, R. B., Brooks, J. D., et al. (2024) · Frontiers in Bioinformatics · doi:10.3389/fbinf.2023.1296667 · Cited by 10 · see citing works
- Authors
- Kiemen, A. L., Braxton, A. M., Grahn, M. P., Han, K. S., Babu, J. M., Reichel, R., Jiang, A. C., Kim, B., Hsu, J., Amoa, F., Reddy, S., Hong, S.-M., Cornish, T. C., Thompson, E. D., Huang, P., Wood, L. D., Hruban, R. H., Wirtz, D., & Wu, P.-H.
- Affiliations
- Johns Hopkins University (US)
- Asan Medical Center (KR)
- University of Colorado Anschutz (US)
- Corresponding author
- Wirtz, Denis
- ORCID
- Venue
- Nature Methods
- Published
- 2022-10-24
- Volume
- 19
- Issue
- 11
- Pages
- 1490-1499
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC10500590
- OpenAlex
- W4307286999
- Cited by
- 218
- References
- 70
- Citations by year
- 2026: 41 · 2025: 59 · 2024: 52 · 2023: 34 · 2022: 19 · 2021: 12 · 2020: 1
- FWCI
- 18.19
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature Methods (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Foundation for the National Institutes of Health (U54CA268083, 5T32CA153952, U52CA210173, U01AG060903)
- The Sol Goldman Pancreatic Cancer Research Center
- ARCS Foundation, Inc, Susan Wojcicki and Dennis Troper, The Sol Goldman Pancreatic Cancer Research Center
- The Sol Goldman Pancreatic Cancer Research Center, Susan Wojcicki and Dennis Troper, The Rolfe Foundation for Pancreatic Cancer Research, Allegheny Health Network – Johns Hopkins Cancer Research Fund
- The Sol Goldman Pancreatic Cancer Research Center, Susan Wojcicki and Dennis Troper
- The Sol Goldman Pancreatic Cancer Research Center, NVIDIA GPU Grant
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Cell Image Analysis Techniques
- Physical Sciences › Computer Science › Artificial Intelligence › AI in cancer detection
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Medical Image Segmentation Techniques
- Keywords
- coda, 3D tissue reconstruction, subcellular resolution, serial sectioning, H&E staining, pancreatic cancer, pancreatic ductal system, pancreatic precancerous lesions, carcinogenesis, tissue microstructure, collagen fiber alignment, tissue labeling, high-content imaging
- MeSH terms
- Humans, Pancreas, Pancreatic Neoplasms, Imaging, Three-Dimensional
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review