OBSERVE: guidelines for the refinement of rodent cancer models

Stéphanie I. De Vleeschauwer, Marieke van de Ven, Anaïs Oudin, Karlijn Debusschere, Kate Connor, Annette T. Byrne, Doreen Ram, Anne Marie Rhebergen, Yannick D. Raeves, Maik Dahlhoff, Virginie Dangles-Marie, Els R. Hermans

Published: 2024-07-10 DOI: 10.1038/s41596-024-00998-w

['OBSERVE guidelines', 'rodent cancer models', 'refinement', '3Rs', 'clinical signs']

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Supplementary information

Supplementary Information

Supplementary Note

Generation of mouse–human chimeric embryos

Genome-wide quantification of transcription factor binding at single-DNA-molecule resolution using methyl-transferase footprinting

Generation of CRISPR–Cas9-mediated genetic knockout human intestinal tissue–derived enteroid lines by lentivirus transduction and single-cell cloning

A puromycin-dependent activity-based sensing probe for histochemical staining of hydrogen peroxide in cells and animal tissues

Decoding personal biotic and abiotic airborne exposome

A clinically relevant model of focal embolic cerebral ischemia by thrombus and thrombolysis in rhesus monkeys

Bioengineering human intestinal mucosal grafts using patient-derived organoids, fibroblasts and scaffolds

Biomimetic tail-to-head terpene cyclizations using the resorcin[4]arene capsule catalyst

Neuroscience robotics for controlled induction and real-time assessment of hallucinations

Scanorama: integrating large and diverse single-cell transcriptomic datasets

Single-cell RNA sequencing (scRNA-seq)（单细胞RNA测序）

Data integration（数据集成）

Heterogeneity（异质性）

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References

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EU Parliament event on animal research. European Animal Resarch Association http://www.eara.eu/post/eu-parliament-event-on-animal-research (2022).
Russell, W. M. S. & Burch, R. L. The Principles of Humane Experimental Technique. (Methuen, 1959).
Tannenbaum, J. & Bennett, B. T. Russell and Burch’s 3Rs then and now: the need for clarity in definition and purpose. J. Am. Assoc. Lab. Anim. Sci. 54, 120–132 (2015).
Hayakawa, Y. et al. Mouse models of gastric cancer. Cancers 5, 92–130 (2013).
O’Brien, S. G. et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N. Engl. J. Med. 348, 994–1004 (2003).
Fazio, M., Ablain, J., Chuan, Y., Langenau, D. M. & Zon, L. I. Zebrafish patient avatars in cancer biology and precision cancer therapy. Nat. Rev. Cancer 20, 263–273 (2020).
Pauli, C. et al. Personalized in vitro and in vivo cancer models to guide precision medicine. Cancer Discov. 7, 462–477 (2017).
Le Magnen, C., Dutta, A. & Abate-Shen, C. Optimizing mouse models for precision cancer prevention. Nat. Rev. Cancer 16, 187––196 (2016).
Animals used for scientific purposes. European Commission http://ec.europa.eu/environment/chemicals/lab_animals/alures_en.htm (2022).
Guillen, K. P. et al. A human breast cancer-derived xenograft and organoid platform for drug discovery and precision oncology. Nat. Cancer 3, 232–250 (2022).
Honkala, A., Malhotra, S. V., Kummar, S. & Junttila, M. R. Harnessing the predictive power of preclinical models for oncology drug development. Nat. Rev. Drug Discov. 21, 99–114 (2022).
Cuppens, T. et al. Potential targets’ analysis reveals dual PI3K/mTOR pathway inhibition as a promising therapeutic strategy for uterine leiomyosarcomas—an ENITEC group initiative. Clin. Cancer Res. 23, 1274–1285 (2017).
Hebert, J. D., Neal, J. W. & Winslow, M. M. Dissecting metastasis using preclinical models and methods. Nat. Rev. Cancer 23, 391–407 (2023).
Perse, M. Cisplatin mouse models: treatment, toxicity and Translatability. Biomedicines 9, 1406 (2021).
Karkampouna, S. et al. Patient-derived xenografts and organoids model therapy response in prostate cancer. Nat. Commun. 12, 1117 (2021).
Patton, E. E. et al. Melanoma models for the next generation of therapies. Cancer Cell 39, 610–631 (2021).
Zitvogel, L., Pitt, J. M., Daillere, R., Smyth, M. J. & Kroemer, G. Mouse models in oncoimmunology. Nat. Rev. Cancer 16, 759–773 (2016).
Gardner, E. E. & Rudin, C. M. Drug therapy: preclinical oncology—reporting transparency needed. Nat. Rev. Clin. Oncol. 13, 8–9 (2016).
Amaral, O. B. & Neves, K. Reproducibility: expect less of the scientific paper. Nature 597, 329–331 (2021).
Pritt, S. L. & Hammer, R. E. The interplay of ethics, animal welfare, and IACUC oversight on the reproducibility of animal studies. Comp. Med. 67, 101–105 (2017).
Cheleuitte-Nieves, C. & Lipman, N. S. Improving replicability, reproducibility, and reliability in preclinical research: a shared responsibility. ILAR J. 60, 113–119 (2019).
Errington, T. M. et al. Investigating the replicability of preclinical cancer biology. eLife 10, e.71601 (2021).
Smith, A. J., Clutton, R. E., Lilley, E., Hansen, K. E. A. & Brattelid, T. PREPARE: guidelines for planning animal research and testing. Lab. Anim. 52, 135–141 (2018).
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M. & Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412 (2010).
Percie du Sert, N. et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PloS Biol. 18, e3000410 (2020).
Workman, P. et al. Guidelines for the welfare and use of animals in cancer research. Br. J. Cancer 102, 1555–1577 (2010).
Wallace, J. Humane endpoints and cancer research. ILAR J. 41, 87–93 (2000).
Workman, P. et al. UKCCCR guidelines for the welfare of animals in experimental neoplasia. Lab. Anim. 22, 195–201 (1988).
Winn, C. B. et al. Automated monitoring of respiratory rate as a novel humane endpoint: a refinement in mouse metastatic lung cancer models. PLoS ONE 16, e0257694 (2021).
Aldred, A. J., Cha, M. C. & Meckling-Gill, K. A. Determination of a humane endpoint in the L1210 model of murine leukemia. Contemp. Top. Lab. Anim. Sci. 41, 24–27 (2002).
Paster, E. V., Villines, K. A. & Hickman, D. L. Endpoints for mouse abdominal tumor models: refinement of current criteria. Comp. Med. 59, 234–241 (2009).
Helgers, S. O. A. et al. Body weight algorithm predicts humane endpoint in an intracranial rat glioma model. Sci. Rep. 10, 9020 (2020).
Oliveira, M. et al. Implementation of humane endpoints in a urinary bladder carcinogenesis study in rats. Vivo 31, 1073–1080 (2017).
Silva-Reis, R. et al. Refinement of animal model of colorectal carcinogenesis through the definition of novel humane endpoints. Animals 11, 985 (2021).
Akladios, C., Ignat, M., Mutter, D. & Aprahamian, M. Survival variability of controls and definition of imaging endpoints for longitudinal follow-up of pancreatic ductal adenocarcinoma in rats. J. Cancer Res. Clin. Oncol. 143, 29–34 (2017).
Kobaek-Larsen, M., Rud, L., Oestergaard Soerensen, F. & Ritskes-Hoitinga, J. Laparoscopy of rats with experimental liver metastases: a method to assess new humane endpoints. Lab. Anim. 38, 162–168 (2004).
Percie du Sert, N. et al. The IMPROVE guidelines (ischaemia models: procedural refinements of in vivo experiments). J. Cereb. Blood Flow. Metab. 37, 3488–3517 (2017).
Mirzoyan, Z. et al. Drosophila melanogaster: a model organism to study cancer. Front. Genet. 10, 51 (2019).
Yamamura, R., Ooshio, T. & Sonoshita, M. Tiny Drosophila makes giant strides in cancer research. Cancer Sci. 112, 505–514 (2021).
Robertson, N., Schook, L. B. & Schachtschneider, K. M. Porcine cancer models: potential tools to enhance cancer drug trials. Expert Opin. Drug Discov. 15, 893–902 (2020).
Oh, J. H. & Cho, J. Y. Comparative oncology: overcoming human cancer through companion animal studies. Exp. Mol. Med. 55, 725–734 (2023).
Deycmar, S., Gomes, B., Charo, J., Ceppi, M. & Cline, J. M. Spontaneous, naturally occurring cancers in non-human primates as a translational model for cancer immunotherapy. J. Immunother. Cancer 11, e005514 (2023).
Cannon, C. M. Cats, cancer and comparative oncology. Vet. Sci. 2, 111–126 (2015).
Overgaard, N. H. et al. Of mice, dogs, pigs, and men: choosing the appropriate model for immuno-oncology research. ILAR J. 59, 247–262 (2018).
LeBlanc, A. K. & Mazcko, C. N. Improving human cancer therapy through the evaluation of pet dogs. Nat. Rev. Cancer 20, 727–742 (2020).
Schook, L. B. et al. A genetic porcine model of cancer. PLoS ONE 10, e0128864 (2015).
Kalla, D. et al. The missing link: cre pigs for cancer research. Front. Oncol. 11, 755746 (2021).
Kalla, D., Kind, A. & Schnieke, A. Genetically engineered pigs to study cancer. Int. J. Mol. Sci. 21, 488 (2020).
Astell, K. R. & Sieger, D. Zebrafish in vivo models of cancer and metastasis. Cold Spring Harb. Perspect. Med. 10, a037077 (2020).
Jiang, H., Kimura, T., Hai, H., Yamamura, R. & Sonoshita, M. Drosophila as a toolkit to tackle cancer and its metabolism. Front. Oncol. 12, 982751 (2022).
Hendricks-Wenger, A. et al. Employing novel porcine models of subcutaneous pancreatic cancer to evaluate oncological therapies. Methods Mol. Biol. 2394, 883–895 (2022).
Callesen, M. M. et al. A genetically inducible porcine model of intestinal cancer. Mol. Oncol. 11, 1616–1629 (2017).
Boas, F. E. et al. Induction and characterization of pancreatic cancer in a transgenic pig model. PLoS ONE 15, e0239391 (2020).
Saur, D. & Schnieke, A. Porcine cancer models for clinical translation. Nat. Rev. Cancer 22, 375–376 (2022).
Jarvis, S. et al. Non-rodent animal models of osteosarcoma: a review. Cancer Treat. Res. Commun. 27, 100307 (2021).
Penet, M. F. et al. Ascites volumes and the ovarian cancer microenvironment. Front. Oncol. 8, 595 (2018).
Sale, S. & Orsulic, S. Models of ovarian cancer metastasis: murine models. Drug Discov. Today Dis. Models 3, 149––154 (2006).
Zakarya, R., Howell, V. M. & Colvin, E. K. Modelling epithelial ovarian cancer in mice: classical and emerging approaches. Int. J. Mol. Sci. 21, 4806 (2020).
Ehlich, H. et al. INFRAFRONTIER quality principles in systemic phenotyping. Mamm., Genome 33, 120–122 (2022).
Meehan, T. F. et al. PDX-MI: minimal information for patient-derived tumor xenograft models. Cancer Res. 77, e62–e66 (2017).
Peterson, N. C. From bench to cageside: risk assessment for rodent pathogen contamination of cells and biologics. ILAR J. 49, 310–315 (2008).
Nicklas, W., Kraft, V. & Meyer, B. Contamination of transplantable tumors, cell lines, and monoclonal antibodies with rodent viruses. Lab. Anim. Sci. 43, 296–300 (1993).
Geraghty, R. J. et al. Guidelines for the use of cell lines in biomedical research. Br. J. Cancer 111, 1021–1046 (2014).
Chateau-Joubert, S. et al. Spontaneous mouse lymphoma in patient-derived tumor xenografts: the importance of systematic analysis of xenografted human tumor tissues in preclinical efficacy trials. Transl. Oncol. 14, 101133 (2021).
Diehl, K. H. et al. A good practice guide to the administration of substances and removal of blood, including routes and volumes. J. Appl. Toxicol. 21, 15–23 (2001).
Turner, P. V., Brabb, T., Pekow, C. & Vasbinder, M. A. Administration of substances to laboratory animals: routes of administration and factors to consider. J. Am. Assoc. Lab. Anim. Sci. 50, 600–613 (2011).
Glascock, J. J. et al. Delivery of therapeutic agents through intracerebroventricular (ICV) and intravenous (IV) injection in mice. J. Vis. Exp. http://doi.org/10.3791/2968 (2011).
Blair-Handon, R., Mueller, K. & Hoogstraten-Miller, S. An alternative method for intrathymic injections in mice. Lab. Anim. 39, 248–252 (2010).
Okano, M. et al. Orthotopic implantation achieves better engraftment and faster growth than subcutaneous implantation in breast cancer patient-derived xenografts. J. Mammary Gland Biol. Neoplasia 25, 27–36 (2020).
Rashid, O. M. et al. An improved syngeneic orthotopic murine model of human breast cancer progression. Breast Cancer Res. Treat. 147, 501–512 (2014).
Zhang, G. L., Zhang, Y., Cao, K. X. & Wang, X. M. Orthotopic injection of breast cancer cells into the mice mammary fat pad. J. Vis. Exp. http://doi.org/10.3791/58604 (2019).
Byrne, A. T. et al. Interrogating open issues in cancer precision medicine with patient-derived xenografts. Nat. Rev. Cancer 17, 254–268 (2017).
Tavera-Mendoza, L. E. & Brown, M. A less invasive method for orthotopic injection of breast cancer cells into the mouse mammary gland. Lab. Anim. 51, 85–88 (2017).
Katsuta, E. et al. Modified breast cancer model for preclinical immunotherapy studies. J. Surg. Res. 204, 467–474 (2016).
Martinez-Sabadell, A., Ovejero Romero, P., Arribas, J. & Arenas, E. J. Protocol to generate a patient derived xenograft model of acquired resistance to immunotherapy in humanized mice. STAR Protoc. 3, 101712 (2022).
Krause, S., Brock, A. & Ingber, D. E. Intraductal injection for localized drug delivery to the mouse mammary gland. J. Vis. Exp. http://doi.org/10.3791/50692 (2013).
Bu, W. & Li, Y. Intraductal injection of lentivirus vectors for stably introducing genes into rat mammary epithelial cells in vivo. J. Mammary Gland Biol. Neoplasia 25, 389–396 (2020).
Barahona, M. J., Rojas, J., Uribe, E. A. & Garcia-Robles, M. A. Tympanic membrane rupture during stereotaxic surgery disturbs the normal feeding behavior in rats. Front. Behav. Neurosci. 14, 591204 (2020).
Ferry, B. & Gervasoni, D. Improving stereotaxic neurosurgery techniques and procedures greatly reduces the number of rats used per experimental group—a practice report. Animals 11, 2662 (2021).
Irtenkauf, S. M. et al. Optimization of glioblastoma mouse orthotopic xenograft models for translational research. Comp. Med. 67, 300–314 (2017).
Onn, A. et al. Development of an orthotopic model to study the biology and therapy of primary human lung cancer in nude mice. Clin. Cancer Res. 9, 5532–5539 (2003).
Boehle, A. S., Dohrmann, P., Leuschner, I., Kalthoff, H. & Henne-Bruns, D. An improved orthotopic xenotransplant procedure for human lung cancer in SCID bg mice. Ann. Thorac. Surg. 69, 1010–1015 (2000).
Kang, Y. et al. Development of an orthotopic transplantation model in nude mice that simulates the clinical features of human lung cancer. Cancer Sci. 97, 996–1001 (2006).
Buckle, T. & van Leeuwen, F. W. Validation of intratracheal instillation of lung tumour cells in mice using single photon emission computed tomography/computed tomography imaging. Lab. Anim. 44, 40–45 (2010).
Nakajima, T. et al. Orthotopic lung cancer murine model by nonoperative transbronchial approach. Ann. Thorac. Surg. 97, 1771–1775 (2014).
Das, S., MacDonald, K., Chang, H. Y. & Mitzner, W. A simple method of mouse lung intubation. J. Vis. Exp. 73, e50318 (2013).
Brown, R. H., Walters, D. M., Greenberg, R. S. & Mitzner, W. A method of endotracheal intubation and pulmonary functional assessment for repeated studies in mice. J. Appl. Physiol. 87, 2362–2365 (1999).
Roughan, J. V., Bertrand, H. G. & Isles, H. M. Meloxicam prevents COX-2-mediated post-surgical inflammation but not pain following laparotomy in mice. Eur. J. Pain. 20, 231–240 (2016).
Kashtan, H. et al. Intra-rectal injection of tumour cells: a novel animal model of rectal cancer. Surg. Oncol. 1, 251–256 (1992).
Richon, S., Zajac, O., Perez Gonzalez, C. & Matic Vignjevic, D. Optimized protocol for the generation of an orthotopic colon cancer mouse model and metastasis. STAR Protoc. 4, 102022 (2023).
Zigmond, E. et al. Utilization of murine colonoscopy for orthotopic implantation of colorectal cancer. PLoS ONE 6, e28858 (2011).
Hite, N. et al. An optimal orthotopic mouse model for human colorectal cancer primary tumor growth and spontaneous metastasis. Dis. Colon Rectum 61, 698–705 (2018).
McVeigh, L. E. et al. Development of orthotopic tumour models using ultrasound-guided intrahepatic injection. Sci. Rep. 9, 9904 (2019).
Huynh, A. S. et al. Development of an orthotopic human pancreatic cancer xenograft model using ultrasound guided injection of cells. PLoS ONE 6, e20330 (2011).
Camara Serrano, J. A. Ultrasound guided surgery as a refinement tool in oncology research. Animals 12, 3445 (2022).
RA, V. A. N. N. et al. Tissue-directed implantation using ultrasound visualization for development of biologically relevant metastatic tumor xenografts. Vivo 31, 779–791 (2017).
Jager, W. et al. Ultrasound-guided intramural inoculation of orthotopic bladder cancer xenografts: a novel high-precision approach. PLoS ONE 8, e59536 (2013).
Hadaschik, B. A. et al. A validated mouse model for orthotopic bladder cancer using transurethral tumour inoculation and bioluminescence imaging. BJU Int. 100, 1377–1384 (2007).
Watanabe, T. et al. An improved intravesical model using human bladder cancer cell lines to optimize gene and other therapies. Cancer Gene Ther. 7, 1575–1580 (2000).
Yardeni, T., Eckhaus, M., Morris, H. D., Huizing, M. & Hoogstraten-Miller, S. Retro-orbital injections in mice. Lab. Anim. 40, 155–160 (2011).
Leon-Rico, D. et al. Comparison of haematopoietic stem cell engraftment through the retro-orbital venous sinus and the lateral vein: alternative routes for bone marrow transplantation in mice. Lab. Anim. 49, 132–141 (2015).
Li, Q. et al. Analyses of very early hemopoietic regeneration after bone marrow transplantation: comparison of intravenous and intrabone marrow routes. Stem Cells 25, 1186–1194 (2007).
Kushida, T. et al. Intra-bone marrow injection of allogeneic bone marrow cells: a powerful new strategy for treatment of intractable autoimmune diseases in MRL/lpr mice. Blood 97, 3292–3299 (2001).
Sawyer, G. J. et al. Cardiovascular function following acute volume overload for hydrodynamic gene delivery to the liver. Gene Ther. 14, 1208–1217 (2007).
Suda, T., Gao, X., Stolz, D. B. & Liu, D. Structural impact of hydrodynamic injection on mouse liver. Gene Ther. 14, 129–137 (2007).
Campbell, J. P., Merkel, A. R., Masood-Campbell, S. K., Elefteriou, F. & Sterling, J. A. Models of bone metastasis. J. Vis. Exp. 4, e4260 (2012).
Zhou, H. & Zhao, D. Ultrasound imaging-guided intracardiac injection to develop a mouse model of breast cancer brain metastases followed by longitudinal MRI. J. Vis. Exp. http://doi.org/10.3791/51146 (2014).
Stocking, K. L. et al. Use of low-molecular-weight heparin to decrease mortality in mice after intracardiac injection of tumor cells. Comp. Med. 59, 37–45 (2009).
Gehling, A. M. et al. evaluation of volume of intramuscular injection into the caudal thigh muscles of female and male BALB/c mice (Mus musculus). J. Am. Assoc. Lab. Anim. Sci. 57, 35–43 (2018).
Pfeiffenberger, U. et al. Assessment and refinement of intra-bone marrow transplantation in mice. Lab. Anim. 49, 121–131 (2015).
Uluckan, O., Segaliny, A., Botter, S., Santiago, J. M. & Mutsaers, A. J. Preclinical mouse models of osteosarcoma. Bonekey Rep. 4, 670 (2015).
Abel, E. L., Angel, J. M., Kiguchi, K. & DiGiovanni, J. Multi-stage chemical carcinogenesis in mouse skin: fundamentals and applications. Nat. Protoc. 4, 1350–1362 (2009).
Levin-Allerhand, J. A., Sokol, K. & Smith, J. D. Safe and effective method for chronic 17beta-estradiol administration to mice. Contemp. Top. Lab. Anim. Sci. 42, 33–35 (2003).
Tolba, R., Kraus, T., Liedtke, C., Schwarz, M. & Weiskirchen, R. Diethylnitrosamine (DEN)-induced carcinogenic liver injury in mice. Lab. Anim. 49, 59–69 (2015).
Zeng, L., Li, W. & Chen, C. S. Breast cancer animal models and applications. Zool. Res. 41, 477–494 (2020).
Rivina, L., Davoren, M. J. & Schiestl, R. H. Mouse models for radiation-induced cancers. Mutagenesis 31, 491–509 (2016).
Scholten, D., Trebicka, J., Liedtke, C. & Weiskirchen, R. The carbon tetrachloride model in mice. Lab. Anim. 49, 4–11 (2015).
Duran-Struuck, R. & Dysko, R. C. Principles of bone marrow transplantation (BMT): providing optimal veterinary and husbandry care to irradiated mice in BMT studies. J. Am. Assoc. Lab. Anim. Sci. 48, 11–22 (2009).
Tang, B., Foss, K., Lichtor, T., Phillips, H. & Roy, E. Resection of orthotopic murine brain glioma. Neuroimmunol. Neuroinflamm. 8, 64–69 (2021).
Gast, C. E., Shaw, A. K., Wong, M. H. & Coussens, L. M. Surgical procedures and methodology for a preclinical murine model of de novo mammary cancer metastasis. J. Vis. Exp. http://doi.org/10.3791/54852 (2017).
Ren, L., Huang, S., Beck, J. & LeBlanc, A. K. Impact of limb amputation and cisplatin chemotherapy on metastatic progression in mouse models of osteosarcoma. Sci. Rep. 11, 24435 (2021).
Mallya, K., Gautam, S. K., Aithal, A., Batra, S. K. & Jain, M. Modeling pancreatic cancer in mice for experimental therapeutics. Biochim. Biophys. Acta Rev. Cancer 1876, 188554 (2021).
Linxweiler, J. et al. Primary tumor resection decelerates disease progression in an orthotopic mouse model of metastatic prostate cancer. Cancers 14, 737 (2022).
Sweeney, K. J. et al. Validation of an imageable surgical resection animal model of glioblastoma (GBM). J. Neurosci. Methods 233, 99–104 (2014).
Chuprin, J. et al. Humanized mouse models for immuno-oncology research. Nat. Rev. Clin. Oncol. 20, 192–206 (2023).
Deboer, M. D. Animal models of anorexia and cachexia. Expert Opin. Drug Discov. 4, 1145–1155 (2009).
Bennani-Baiti, N. & Walsh, D. Animal models of the cancer anorexia–cachexia syndrome. Support Care Cancer 19, 1451–1463 (2011).
Euhus, D. M., Hudd, C., LaRegina, M. C. & Johnson, F. E. Tumor measurement in the nude mouse. J. Surg. Oncol. 31, 229–234 (1986).
Tomayko, M. M. & Reynolds, C. P. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol. 24, 148–154 (1989).
Ishida, K. et al. Current mouse models of oral squamous cell carcinoma: genetic and chemically induced models. Oral. Oncol. 73, 16–20 (2017).
Naik, K. et al. The histopathology of oral cancer pain in a mouse model and a human cohort. J. Dent. Res. 100, 194–200 (2021).
Pacharinsak, C. & Beitz, A. Animal models of cancer pain. Comp. Med. 58, 220–233 (2008).
Pineda-Farias, J. B., Saloman, J. L. & Scheff, N. N. Animal models of cancer-related pain: current perspectives in translation. Front. Pharmacol. 11, 610894 (2020).
Tetreault, M. P. Esophageal cancer: insights from mouse models. Cancer Growth Metastasis 8, 37–46 (2015).
Cardesa, A., Ovelar, M. Y. & Pera, M. in Digestive System (eds Carlyle Jones, T., Popp, J. A. & Mohr, U.) 318–322 (Springer Berlin, 1997).
Hu, H. et al. Real-time bioluminescence and tomographic imaging of gastric cancer in a novel orthotopic mouse model. Oncol. Rep. 27, 1937–1943 (2012).
Fish, R., Danneman, P. J., Brown, M. & Karas, A. Anesthesia and Analgesia in Laboratory Animals (Academic Press, 2011).
Bhargava, S., Hotz, B., Buhr, H. J. & Hotz, H. G. An orthotopic nude mouse model for preclinical research of gastric cardia cancer. Int. J. Colorectal Dis. 24, 31–39 (2009).
Liu, S. et al. Dynamic observation of the progression of chronic gastritis to gastric cancer in a disease–TCM pattern rat model. J. Trad. Chin. Med. Sci. 8, 124–134 (2021).
Herreros-Villanueva, M., Hijona, E., Cosme, A. & Bujanda, L. Mouse models of pancreatic cancer. World J. Gastroenterol. 18, 1286–1294 (2012).
Lwin, T. M. et al. Fluorescent humanized anti-CEA antibody specifically labels metastatic pancreatic cancer in a patient-derived orthotopic xenograft (PDOX) mouse model. Oncotarget 9, 37333–37342 (2018).
Becker, C. et al. In vivo imaging of colitis and colon cancer development in mice using high resolution chromoendoscopy. Gut 54, 950–954 (2005).
Hasty, P. et al. eRapa restores a normal life span in a FAP mouse model. Cancer Prev. Res. 7, 169–178 (2014).
Chartier, L. C., Hebart, M. L., Howarth, G. S., Whittaker, A. L. & Mashtoub, S. Affective state determination in a mouse model of colitis-associated colorectal cancer. PLoS ONE 15, e0228413 (2020).
Ikenoue, T. et al. A novel mouse model of intrahepatic cholangiocarcinoma induced by liver-specific Kras activation and Pten deletion. Sci. Rep. 6, 23899 (2016).
Vogt, A. et al. Alpha-fetoprotein- and CD40 ligand-expressing dendritic cells for immunotherapy of hepatocellular carcinoma. Cancers 13, 3375 (2021).
Chen, Z., Li, S., Han, L. & He, X. Optimized protocol for an inducible rat model of liver tumor with chronic hepatocellular injury, inflammation, fibrosis, and cirrhosis. STAR Protoc. 2, 100353 (2021).
Odashima, S. Comparative studies on the transplantability of liver cancers induced in rats fed with 3′-methyl-4-dimethylaminoazobenzene for 3–6 months. Gan 53, 325–348 (1962).
Pretto, F. et al. Sunitinib prevents cachexia and prolongs survival of mice bearing renal cancer by restraining STAT3 and MuRF-1 activation in muscle. Oncotarget 6, 3043–3054 (2015).
Roughan, J. V., Coulter, C. A., Flecknell, P. A., Thomas, H. D. & Sufka, K. J. The conditioned place preference test for assessing welfare consequences and potential refinements in a mouse bladder cancer model. PLoS ONE 9, e103362 (2014).
Naito, T., Higuchi, T., Shimada, Y. & Kakinuma, C. An improved mouse orthotopic bladder cancer model exhibiting progression and treatment response characteristics of human recurrent bladder cancer. Oncol. Lett. 19, 833–839 (2020).
Philyppov, I. B. et al. Alterations in detrusor contractility in rat model of bladder cancer. Sci. Rep. 10, 19651 (2020).
Xiao, Z. et al. Characterization of a novel transplantable orthotopic rat bladder transitional cell tumour model. Br. J. Cancer 81, 638––646 (1999).
Ding, J. et al. Current animal models of bladder cancer: awareness of translatability (review). Exp. Ther. Med. 8, 691–699 (2014).
Senapati, S. et al. Overexpression of macrophage inhibitory cytokine-1 induces metastasis of human prostate cancer cells through the FAK–RhoA signaling pathway. Oncogene 29, 1293–1302 (2010).
Pang, K. et al. Monitoring circulating prostate cancer cells by in vivo flow cytometry assesses androgen deprivation therapy on metastasis. Cytom. A 93, 517–524 (2018).
De Ciantis, P. D., Yashpal, K., Henry, J. & Singh, G. Characterization of a rat model of metastatic prostate cancer bone pain. J. Pain. Res. 3, 213–221 (2010).
Bosland, M. C., Schlicht, M. J., Horton, L. & McCormick, D. L. The MNU plus testosterone rat model of prostate carcinogenesis. Toxicol. Pathol. 50, 478–496 (2022).
Flecknell, P. Laboratory Animal Anaesthesia (Academic Press, 2015).
Haldorsen, I. S. et al. Multimodal imaging of orthotopic mouse model of endometrial carcinoma. PLoS ONE 10, e0135220 (2015).
Baert, T. et al. The dark side of ID8-Luc2: pitfalls for luciferase tagged murine models for ovarian cancer. J. Immunother. Cancer 3, 57 (2015).
Rose, G. S. et al. Development and characterization of a clinically useful animal model of epithelial ovarian cancer in the Fischer 344 rat. Am. J. Obstet. Gynecol. 175, 593–599 (1996).
He, C. et al. A human papillomavirus-independent cervical cancer animal model reveals unconventional mechanisms of cervical carcinogenesis. Cell Rep. 26, 2636–2650 e2635 (2019).
Henkle, T. R. et al. Development of a novel mouse model of spontaneous high-risk hpve6/e7-expressing carcinoma in the cervicovaginal tract. Cancer Res. 81, 4560–4569 (2021).
Hamada, K., Ueda, N., Ito, M., Roth, J. A. & Follen, M. The nude rat as an orthotopic model for cervical cancer. Gynecol. Oncol. 99, S159–S165 (2005).
Koutcher, J. A. et al. MRI of mouse models for gliomas shows similarities to humans and can be used to identify mice for preclinical trials. Neoplasia 4, 480–485 (2002).
Bouckaert, C. et al. Development of a rat model for glioma-related epilepsy. Int. J. Mol. Sci. 21, 6999 (2020).
Nagarajan, P. P. et al. Lentiviral-induced spinal cord gliomas in rat model. Int. J. Mol. Sci. 22, 12943 (2021).
Shimoyama, M., Tanaka, K., Hasue, F. & Shimoyama, N. A mouse model of neuropathic cancer pain. Pain 99, 167–174 (2002).
Mao-Ying, Q.-L. et al. A rat model of bone cancer pain induced by intra-tibia inoculation of Walker 256 mammary gland carcinoma cells. Biochem. Biophys. Res. Commun. 345, 1292–1298 (2006).
Yang, H. et al. Proteomic analysis of spinal cord tissue in a rat model of cancer-induced bone pain. Front. Mol. Neurosci. 15, 1009615 (2022).
Gelbard, A. et al. An orthotopic murine model of sinonasal malignancy. Clin. Cancer Res. 14, 7348–7357 (2008).
Feron, V. J., Woutersen, R. A., van Garderen-Hoetmer, A. & Dreef-van der Meulen, H. C. Upper respiratory tract tumors in Cpb:WU (Wistar random) rats. Environ. Health Perspect. 85, 305–315 (1990).
Miller, A. L. & Roughan, J. V. Welfare assessment, end-point refinement and the effects of non-aversive handling in C57BL/6 mice with Lewis lung cancer. Animals http://doi.org/10.3390/ani12010023 (2021).
Mendoza, A. et al. A novel noninvasive method for evaluating experimental lung metastasis in mice. J. Am. Assoc. Lab. Anim. Sci. 52, 584–589 (2013).
Byhardt, R. W., Almagro, U. A., Fish, B. L. & Moulder, J. E. Development of a rat lung cancer model. Int. J. Radiat. Oncol. Biol. Phys. 10, 2125–2130 (1984).
Zhu, X. C. et al. Analgesic effects of lappaconitine in leukemia bone pain in a mouse model. PeerJ 3, e936 (2015).
Helseth, A., Siegal, G. P., Haug, E. & Bautch, V. L. Transgenic mice that develop pituitary tumors. a model for Cushing’s disease. Am. J. Pathol. 140, 1071–1080 (1992).
Chang-Wei, H., Li, Y. B., Han, X. Y., Yin, G. F. & Wang, X. R. To explore the change of motor cognitive function in pituitary tumor rats after operation. Comput. Assist. Surg. 28, 2198099 (2023).
Kim, W. G., Park, J. W., Willingham, M. C. & Cheng, S. Y. Diet-induced obesity increases tumor growth and promotes anaplastic change in thyroid cancer in a mouse model. Endocrinology 154, 2936–2947 (2013).
Snarskaya, E. S., Pylev, L. N., Akhunzyanov, A. A. & Kuznetсova, E. V. Experimental basosquamous carcinoma model in rats. BioNanoScience 7, 423–427 (2017).
Stribbling, S. M. & Ryan, A. J. The cell-line-derived subcutaneous tumor model in preclinical cancer research. Nat. Protoc. 17, 2108–2128 (2022).
Ehx, G. et al. Xenogeneic graft-versus-host disease in humanized NSG and NSG-HLA-A2/HHD mice. Front. Immunol. 9, 1943 (2018).
Lai, H. Y., Chou, T. Y., Tzeng, C. H. & Lee, O. K. Cytokine profiles in various graft-versus-host disease target organs following hematopoietic stem cell transplantation. Cell Transplant. 21, 2033–2045 (2012).
Ullman-Cullere, M. H. & Foltz, C. J. Body condition scoring: a rapid and accurate method for assessing health status in mice. Lab. Anim. Sci. 49, 319–323 (1999).
Hickman, D. L. & Swan, M. Use of a body condition score technique to assess health status in a rat model of polycystic kidney disease. J. Am. Assoc. Lab. Anim. Sci. 49, 155–159 (2010).
Burkholder, T., Foltz, C., Karlsson, E., Linton, C. G. & Smith, J. M. Health evaluation of experimental laboratory mice. Curr. Protoc. Mouse Biol. 2, 145–165 (2012).
Raja, S. N. et al. The revised International Association for the Study of Pain definition of pain: concepts, challenges, and compromises. Pain 161, 1976–1982 (2020).
Langford, D. J. et al. Coding of facial expressions of pain in the laboratory mouse. Nat. Methods 7, 447–449 (2010).
Sotocinal, S. G. et al. The Rat Grimace scale: a partially automated method for quantifying pain in the laboratory rat via facial expressions. Mol. Pain. 7, 55 (2011).
Jirkof, P. et al. Assessment of postsurgical distress and pain in laboratory mice by nest complexity scoring. Lab. Anim. 47, 153–161 (2013).
Jirkof, P. et al. Burrowing behavior as an indicator of post-laparotomy pain in mice. Front. Behav. Neurosci. 4, 165 (2010).
Turner, P. V., Pang, D. S. & Lofgren, J. L. A review of pain assessment methods in laboratory rodents. Comp. Med. 69, 451–467 (2019).
Deuis, J. R., Dvorakova, L. S. & Vetter, I. Methods used to evaluate pain behaviors in rodents. Front. Mol. Neurosci. 10, 284 (2017).
Wright-Williams, S. L., Courade, J. P., Richardson, C. A., Roughan, J. V. & Flecknell, P. A. Effects of vasectomy surgery and meloxicam treatment on faecal corticosterone levels and behaviour in two strains of laboratory mouse. Pain 130, 108–118 (2007).
Do, J. P. et al. Automated and continuous monitoring of animal welfare through digital alerting. Comp. Med. 70, 313–327 (2020).
Collins, D. E., Mulka, K. R., Hoenerhoff, M. J., Taichman, R. S. & Villano, J. S. Clinical assessment of urinary tract damage during sustained-release estrogen supplementation in mice. Comp. Med. 67, 11–21 (2017).
Pearse, G., Frith, J., Randall, K. J. & Klinowska, T. Urinary retention and cystitis associated with subcutaneous estradiol pellets in female nude mice. Toxicol. Pathol. 37, 227–234 (2009).
Guyenet, S. J. et al. A simple composite phenotype scoring system for evaluating mouse models of cerebellar ataxia. J. Vis. Exp. http://doi.org/10.3791/1787 (2010).
Gao, X. et al. in Brain Tumors Vol. 158 (ed. Seano, G.) 199–220 (Springer, 2021).
Kelp, A. et al. A novel transgenic rat model for spinocerebellar ataxia type 17 recapitulates neuropathological changes and supplies in vivo imaging biomarkers. J. Neurosci. 33, 9068–9081 (2013).
Bieler, L. et al. Motor deficits following dorsal corticospinal tract transection in rats: voluntary versus skilled locomotion readouts. Heliyon 4, e00540 (2018).
Brough, D. W., Murkin, J. T., Amos, H. E., Smith, A. I. & Turley, K. D. Comparing variability in measurement of subcutaneous tumors in mice using 3D thermal imaging and calipers. Comp. Med. 72, 364–375 (2022).
Jensen, M. M., Jorgensen, J. T., Binderup, T. & Kjaer, A. Tumor volume in subcutaneous mouse xenografts measured by microCT is more accurate and reproducible than determined by 18F-FDG–microPET or external caliper. BMC Med. Imaging 8, 16 (2008).
Czerninski, R., Amornphimoltham, P., Patel, V., Molinolo, A. A. & Gutkind, J. S. Targeting mammalian target of rapamycin by rapamycin prevents tumor progression in an oral-specific chemical carcinogenesis model. Cancer Prev. Res. 2, 27–36 (2009).
Tanaka, T., Kojima, T., Okumura, A., Yoshimi, N. & Mori, H. Alterations of the nucleolar organizer regions during 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in rats. Carcinogenesis 12, 329–333 (1991).
Goetze, R. G. et al. Utilizing high resolution ultrasound to monitor tumor onset and growth in genetically engineered pancreatic cancer models. J. Vis. Exp. http://doi.org/10.3791/56979 (2018).
Glaser, G. et al. Conventional chemotherapy and oncogenic pathway targeting in ovarian carcinosarcoma using a patient-derived tumorgraft. PLoS ONE 10, e0126867 (2015).
Vitetta, E. S. et al. Tumor dormancy and cell signaling. V. Regrowth of the BCL1 tumor after dormancy is established. Blood 89, 4425–4436 (1997).
Bruckner, M. et al. Murine endoscopy for in vivo multimodal imaging of carcinogenesis and assessment of intestinal wound healing and inflammation. J. Vis. Exp. http://doi.org/10.3791/51875 (2014).
Kodani, T. et al. Flexible colonoscopy in mice to evaluate the severity of colitis and colorectal tumors using a validated endoscopic scoring system. J. Vis. Exp. 80, e50843 (2013).
Habibollahi, P. et al. Optical Imaging with a cathepsin B activated probe for the enhanced detection of esophageal adenocarcinoma by dual channel fluorescent upper GI endoscopy. Theranostics 2, 227–234 (2012).
Dassie, E. et al. Detection of fluorescent organic nanoparticles by confocal laser endomicroscopy in a rat model of Barrett’s esophageal adenocarcinoma. Int. J. Nanomed. 10, 6811–6823 (2015).
Wong, G. S. et al. Optical imaging of periostin enables early endoscopic detection and characterization of esophageal cancer in mice. Gastroenterology 144, 294–297 (2013).
El-Masry, O. S. et al. Oral intragastric DMBA administration induces acute lymphocytic leukemia and other tumors in male Wistar rats. J. Exp. Pharmacol. 14, 87–96 (2022).
Tannous, B. A. Gaussia luciferase reporter assay for monitoring biological processes in culture and in vivo. Nat. Protoc. 4, 582–591 (2009).
Delgado-SanMartin, J. et al. An innovative non-invasive technique for subcutaneous tumour measurements. PLoS ONE 14, e0216690 (2019).
Klerk, C. P. et al. Validity of bioluminescence measurements for noninvasive in vivo imaging of tumor load in small animals. Biotechniques 43, 7–13, 30 (2007).
Miller, I. S. et al. Durability of cell line xenograft resection models to interrogate tumor micro-environment targeting agents. Sci. Rep. 9, 9204 (2019).
Jarzabek, M. A. et al. Molecular imaging in the development of a novel treatment paradigm for glioblastoma (GBM): an integrated multidisciplinary commentary. Drug Discov. Today 18, 1052–1066 (2013).
Zeamari, S., Rumping, G., Floot, B., Lyons, S. & Stewart, F. A. In vivo bioluminescence imaging of locally disseminated colon carcinoma in rats. Br. J. Cancer 90, 1259–1264 (2004).
Netufo, O. et al. Refining glioblastoma surgery through the use of intra-operative fluorescence imaging agents. Pharmaceuticals 15, 550 (2022).
Christensen, J., Vonwil, D. & Shastri, V. P. Non-invasive in vivo imaging and quantification of tumor growth and metastasis in rats using cells expressing far-red fluorescence protein. PLoS ONE 10, e0132725 (2015).
Yang, N. et al. A novel GFP nude rat model to investigate tumor-stroma interactions. Cancer Cell Int. 14, 541 (2014).
Hoffman, R. M. Application of GFP imaging in cancer. Lab. Invest. 95, 432–452 (2015).
Marien, E., Hillen, A., Vanderhoydonc, F., Swinnen, J. V. & Vande Velde, G. Longitudinal microcomputed tomography-derived biomarkers for lung metastasis detection in a syngeneic mouse model: added value to bioluminescence imaging. Lab. Invest. 97, 24–33 (2017).
Nota, T. et al. Safety and feasibility of contrast-enhanced computed tomography with a nanoparticle contrast agent for evaluation of diethylnitrosamine-induced liver tumors in a rat model. Acad. Radiol. 30, 30–39 (2023).
Olson, J. D. et al. A gated-7T MRI technique for tracking lung tumor development and progression in mice after exposure to low doses of ionizing radiation. Radiat. Res. 178, 321–327 (2012).
Baier, J. et al. Influence of MRI examinations on animal welfare and study results. Invest. Radiol. 55, 507–514 (2020).
Song, H. T. et al. Rat model of metastatic breast cancer monitored by MRI at 3 tesla and bioluminescence imaging with histological correlation. J. Transl. Med. 7, 88 (2009).
Gui, Q. et al. A new rat model of bone cancer pain produced by rat breast cancer cells implantation of the shaft of femur at the third trochanter level. Cancer Biol. Ther. 14, 193–199 (2013).
Ayers, G. D. et al. Volume of preclinical xenograft tumors is more accurately assessed by ultrasound imaging than manual caliper measurements. J. Ultrasound Med. 29, 891–901 (2010).
Ghaddar, N. et al. Detection of lung tumor progression in mice by ultrasound imaging. J. Vis. Exp. http://doi.org/10.3791/60565 (2020).
Chen, J. Y. et al. Application of high-frequency ultrasound for the detection of surgical anatomy in the rodent abdomen. Vet. J. 191, 246–252 (2012).
O’Farrell, A. C. et al. Implementing systems modelling and molecular imaging to predict the efficacy of BCL-2 inhibition in colorectal cancer patient-derived xenograft models. Cancers 12, 2978 (2020).
Sun, R. et al. A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: an imaging biomarker, retrospective multicohort study. Lancet Oncol. 19, 1180–1191 (2018).
Aubry, K. et al. FDG-PET/CT of head and neck squamous cell carcinoma in a rat model. Mol. Imaging Biol. 11, 88–93 (2009).
Lofgren, J. et al. Analgesics promote welfare and sustain tumour growth in orthotopic 4T1 and B16 mouse cancer models. Lab. Anim. 52, 351–364 (2018).
Husmann, K. et al. Primary tumour growth in an orthotopic osteosarcoma mouse model is not influenced by analgesic treatment with buprenorphine and meloxicam. Lab. Anim. 49, 284–293 (2015).
Taylor, D. K. Influence of pain and analgesia on cancer research studies. Comp. Med. 69, 501–509 (2019).
Strohal, R. et al. Wound management with enzyme alginogels: expert consensus. Hautarzt 68, 36–42 (2017).
Chaudhary, A., Bag, S., Banerjee, P. & Chatterjee, J. Wound healing efficacy of Jamun honey in diabetic mice model through reepithelialization, collagen deposition and angiogenesis. J. Tradit. Complement. Med. 10, 529–543 (2020).
Mitchell, C. M., Salyards, G. W., Theriault, B. R., Langan, G. P. & Luchins, K. R. Evaluation of pain and distress and therapeutic interventions for rectal prolapse in mice to reduce early study removal. J. Am. Assoc. Lab. Anim. Sci. 60, 692–699 (2021).
Foley, P. L., Kendall, L. V. & Turner, P. V. Clinical management of pain in rodents. Comp. Med. 69, 468–489 (2019).

OBSERVE: guidelines for the refinement of rodent cancer models

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