Behavioral, medical imaging and histopathological features of a new rat model of bone cancer pain

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Doré Savard, Louis ^a   Otis, Valerie ^a   Bellevill, Karine ^a   Lemire, Myriam ^a   Archambaul, Mélanie ^b   Tremblay, Luc ^b   Beaudoin, Jean François ^b   Beaudet, Nicolas ^a   Lecomte, Roger ^b   Lepage, Martin ^b   Gendron, Louis ^a   Sarret, Philippe ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; ACTIVATING TRANSCRIPTION FACTOR 3; CALCIUM BINDING PROTEIN; FLUORINE 18; GADOLINIUM PENTETATE; GREEN FLUORESCENT PROTEIN; PROTEIN C FOS; PROTEIN IBA1; SODIUM; TARTARIC ACID; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE CANCER; BONE DENSITY; BONE DESTRUCTION; BONE METASTASIS; BONE REMODELING; CANCER CELL CULTURE; CANCER DIAGNOSIS; CANCER GROWTH; CANCER MODEL; CANCER PAIN; CELL PROLIFERATION; CLINICAL FEATURE; CONTROLLED STUDY; HISTOPATHOLOGY; HYPERALGESIA; IMMUNOREACTIVITY; LUMBAR SPINAL CORD; MALE; MICRO-COMPUTED TOMOGRAPHY; MICROGLIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOCLAST ACTIVITY; OSTEOPENIA; PAIN ASSESSMENT; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; STAINING; ANIMAL; BONE TUMOR; DISEASE MODEL; PAIN; PATHOLOGY; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ANIMALIA; RATTUS;

ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; MAGNETIC RESONANCE IMAGING; MALE; PAIN; POSITRON-EMISSION TOMOGRAPHY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 78149423668     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013774     Document Type: Article

References (85)

1. Coleman RE, Rubens RD (1985) Bone metastases and breast cancer. Cancer Treat Rev 12: 251-270.
2. Coleman RE, Rubens RD (1987) The clinical course of bone metastases from breast cancer. Br J Cancer 55: 61-66.
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA: a cancer journal for clinicians 58: 71-96.
4. Mercadante S, Fulfaro F (2007) Management of painful bone metastases. Current opinion in oncology 19: 308-314.
5. Honore P, Mantyh PW (2000) Bone cancer pain: from mechanism to model to therapy. Pain medicine (Malden, Mass) 1: 303-309.
6. Roato I, Grano M, Brunetti G, Colucci S, Mussa A, et al. (2005) Mechanisms of spontaneous osteoclastogenesis in cancer with bone involvement. FASEB J 19: 228-230.
7. Harvey HA, Cream LR (2007) Biology of bone metastases: causes and consequences. Clinical breast cancer 7 Suppl 1: S7-S13.
8. Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP (2002) Molecular mechanisms of cancer pain. Nature reviews Cancer 2: 201-209.
9. Nagae M, Hiraga T, Yoneda T (2007) Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J Bone Miner Metab 25: 99-104.
10. Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ, et al. (2002) Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 113: 155-166.
11. Honore P, Rogers SD, Schwei MJ, Salak-Johnson JL, Luger NM, et al. (2000) Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 98: 585-598.
12. Kirou-Mauro AM, Hird A, Wong J, Sinclair E, Barnes EA, et al. (2009) Has pain management in cancer patients with bone metastases improved? A seven-year review at an outpatient palliative radiotherapy clinic. J Pain Symptom Manage 37: 77-84.
13. Luger NM, Sabino MA, Schwei MJ, Mach DB, Pomonis JD, et al. (2002) Efficacy of systemic morphine suggests a fundamental difference in the mechanisms that generate bone cancer vs inflammatory pain. Pain 99: 397-406.
14. Nicholson B (2003) Responsible prescribing of opioids for the management of chronic pain. Drugs 63: 17-32.
15. King T, Vardanyan A, Majuta L, Melemedjian O, Nagle R, et al. (2007) Morphine treatment accelerates sarcoma-induced bone pain, bone loss, and spontaneous fracture in a murine model of bone cancer. Pain 132: 154-168.
16. Vestergaard P, Rejnmark L, Mosekilde L (2006) Fracture risk associated with the use of morphine and opiates. J Intern Med 260: 76-87.
17. Clemons MJ, Dranitsaris G, Ooi WS, Yogendran G, Sukovic T, et al. (2006) Phase II trial evaluating the palliative benefit of second-line zoledronic acid in breast cancer patients with either a skeletal-related event or progressive bone metastases despite first-line bisphosphonate therapy. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 24: 4895-4900.
18. Coleman R (2007) Potential use of bisphosphonates in the prevention of metastases in early-stage breast cancer. Clinical breast cancer 7 Suppl 1: S29-35.
19. Lipton A (2007) Efficacy and safety of intravenous bisphosphonates in patients with bone metastases caused by metastatic breast cancer. Clinical breast cancer 7 Suppl 1: S14-20.
20. Ogawa K, Mukai T, Asano D, Kawashima H, Kinuya S, et al. (2007) Therapeutic effects of a 186Re-complex-conjugated bisphosphonate for the palliation of metastatic bone pain in an animal model. J Nucl Med 48: 122-127.
21. Walker K, Medhurst SJ, Kidd BL, Glatt M, Bowes M, et al. (2002) Disease modifying and anti-nociceptive effects of the bisphosphonate, zoledronic acid in a model of bone cancer pain. Pain 100: 219-229.
22. Malden NJ, Pai AY (2007) Oral bisphosphonate associated osteonecrosis of the jaws: three case reports. British dental journal 203: 93-97.
23. Wacnik PW, Eikmeier LJ, Ruggles TR, Ramnaraine ML, Walcheck BK, et al. (2001) Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. The Journal of neuroscience: the official journal of the Society for Neuroscience 21: 9355-9366.
24. Medhurst SJ, Walker K, Bowes M, Kidd BL, Glatt M, et al. (2002) A rat model of bone cancer pain. Pain 96: 129-140.
25. Zwolak P, Dudek AZ, Bodempudi VD, Nguyen J, Hebbel RP, et al. (2008) Local irradiation in combination with bevacizumab enhances radiation control of bone destruction and cancer-induced pain in a model of bone metastases. Int J Cancer 122: 681-688.
26. Mao-Ying QL, Zhao J, Dong ZQ, Wang J, Yu J, et al. (2006) 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.
27. Zhang RX, Liu B, Wang L, Ren K, Qiao JT, et al. (2005) Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia. Pain 118: 125-136.
28. Lee YT (1983) Breast carcinoma: pattern of metastasis at autopsy. J Surg Oncol 23: 175-180.
29. Luger NM, Honore P, Sabino MA, Schwei MJ, Rogers SD, et al. (2001) Osteoprotegerin diminishes advanced bone cancer pain. Cancer research 61: 4038-4047.
30. Schwei MJ, Honore P, Rogers SD, Salak-Johnson JL, Finke MP, et al. (1999) Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. The Journal of neuroscience: the official journal of the Society for Neuroscience 19: 10886-10897.
31. Sabino MA, Luger NM, Mach DB, Rogers SD, Schwei MJ, et al. (2003) Different tumors in bone each give rise to a distinct pattern of skeletal destruction, bone cancer-related pain behaviors and neurochemical changes in the central nervous system. International journal of cancer Journal international du cancer 104: 550-558.
32. Rozel S, Galban CJ, Nicolay K, Lee KC, Sud S, et al. (2009) Synergy between anti-CCL2 and docetaxel as determined by DW-MRI in a metastatic bone cancer model. J Cell Biochem 107: 58-64.
33. Bauerle T, Adwan H, Kiessling F, Hilbig H, Armbruster FP, et al. (2005) Characterization of a rat model with site-specific bone metastasis induced by MDA-MB-231 breast cancer cells and its application to the effects of an antibody against bone sialoprotein. Int J Cancer 115: 177-186.
34. Costelloe CM, Rohren EM, Madewell JE, Hamaoka T, Theriault RL, et al. (2009) Imaging bone metastases in breast cancer: techniques and recommendations for diagnosis. Lancet Oncol 10: 606-614.
35. Omoumi P, Mercier GA, Lecouvet F, Simoni P, Vande Berg BC (2009) CT arthrography, MR arthrography, PET, and scintigraphy in osteoarthritis. Radiol Clin North Am 47: 595-615.
36. Mogil JS (2009) Animal models of pain: progress and challenges. Nat Rev Neurosci 10: 283-294.
37. Harada Y (1975) Induction of metastasizing carcinoma in rats and their biological characteristics. Acta Pathol Jpn 25: 451-461.
38. Watson C, Paxinos G, Kayalioglu G (2009) The Spinal Cord; a Christopher and Dana Reeve foundation text and atlas; Watson C, editor. London: Academic Press. 387 p.
39. Sevcik MA, Luger NM, Mach DB, Sabino MA, Peters CM, et al. (2004) Bone cancer pain: the effects of the bisphosphonate alendronate on pain, skeletal remodeling, tumor growth and tumor necrosis. Pain 111: 169-180.
40. Edoff K, Grenegard M, Hildebrand C (2000) Retrograde tracing and neuropeptide immunohistochemistry of sensory neurones projecting to the cartilaginous distal femoral epiphysis of young rats. Cell Tissue Res 299: 193-200.
41. Schmidt GP, Reiser MF, Baur-Melnyk A (2009) Whole-body imaging of bone marrow. Semin Musculoskelet Radiol 13: 120-133.
42. Vallabhajosula S (2007) (18)F-labeled positron emission tomographic radio-pharmaceuticals in oncology: an overview of radiochemistry and mechanisms of tumor localization. Semin Nucl Med 37: 400-419.
43. Petren-Mallmin M, Andreasson I, Ljunggren O, Ahlstrom H, Bergh J, et al. (1998) Skeletal metastases from breast cancer: uptake of 18F-fluoride measured with positron emission tomography in correlation with CT. Skeletal Radiol 27: 72-76.
44. Schirrmeister H (2007) Detection of bone metastases in breast cancer by positron emission tomography. Radiol Clin North Am 45: 669-676, vi.
45. Coleman RE (2006) Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 12: 6243s-6249s.
46. Canon JR, Roudier M, Bryant R, Morony S, Stolina M, et al. (2008) Inhibition of RANKL blocks skeletal tumor progression and improves survival in a mouse model of breast cancer bone metastasis. Clin Exp Metastasis 25: 119-129.
47. Mouedden ME, Meert TF (2007) Pharmacological evaluation of opioid and non-opioid analgesics in a murine bone cancer model of pain. Pharmacology, biochemistry, and behavior.
48. Niiyama Y, Kawamata T, Yamamoto J, Furuse S, Namiki A (2009) SB366791, a TRPV1 antagonist, potentiates analgesic effects of systemic morphine in a murine model of bone cancer pain. Br J Anaesth 102: 251-258.
49. Menendez L, Lastra A, Hidalgo A, Meana A, Garcia E, et al. (2003) Peripheral opioids act as analgesics in bone cancer pain in mice. Neuroreport 14: 867-869.
50. Hald A, Ding M, Egerod K, Hansen RR, Konradsen D, et al. (2008) Differential effects of repeated low dose treatment with the cannabinoid agonist WIN 55,212-2 in experimental models of bone cancer pain and neuropathic pain. Pharmacol Biochem Behav 91: 38-46.
51. Aloisi AM, Bonifazi M (2006) Sex hormones, central nervous system and pain. Horm Behav 50: 1-7.
52. Cairns BE, Gazerani P (2009) Sex-related differences in pain. Maturitas 63: 292-296.
53. Donovan-Rodriguez T, Dickenson AH, Urch CE (2004) Superficial dorsal horn neuronal responses and the emergence of behavioural hyperalgesia in a rat model of cancer-induced bone pain. Neurosci Lett 360: 29-32.
54. Donovan-Rodriguez T, Dickenson AH, Urch CE (2005) Gabapentin normalizes spinal neuronal responses that correlate with behavior in a rat model of cancer-induced bone pain. Anesthesiology 102: 132-140.
55. Donovan-Rodriguez T, Urch CE, Dickenson AH (2006) Evidence of a role for descending serotonergic facilitation in a rat model of cancer-induced bone pain. Neurosci Lett 393: 237-242.
56. Urch CE, Donovan-Rodriguez T, Dickenson AH (2003) Alterations in dorsal horn neurones in a rat model of cancer-induced bone pain. Pain 106: 347-356.
57. Urch CE, Donovan-Rodriguez T, Gordon-Williams R, Bee LA, Dickenson AH (2005) Efficacy of chronic morphine in a rat model of cancer-induced bone pain: behavior and in dorsal horn pathophysiology. J Pain 6: 837-845.
58. Beyreuther BK, Callizot N, Brot MD, Feldman R, Bain SC, et al. (2007) Antinociceptive efficacy of lacosamide in rat models for tumor- and chemotherapy-induced cancer pain. Eur J Pharmacol 565: 98-104.
59. Fox A, Medhurst S, Courade JP, Glatt M, Dawson J, et al. (2004) Anti-hyperalgesic activity of the cox-2 inhibitor lumiracoxib in a model of bone cancer pain in the rat. Pain 107: 33-40.
60. Mercadante S (1997) Malignant bone pain: pathophysiology and treatment. Pain 69: 1-18.
61. Niv D, Gofeld M, Devor M (2003) Causes of pain in degenerative bone and joint disease: a lesson from vertebroplasty. Pain 105: 387-392.
62. Aebi M (2003) Spinal metastasis in the elderly. Eur Spine J 12 Suppl 2: S202-213.
63. Donthineni R (2009) Diagnosis and staging of spine tumors. Orthop Clin North Am 40: 1-7, v.
64. Mercadante S, Villari P, Ferrera P, Arcuri E, David F (2009) Opioid switching and burst ketamine to improve the opioid response in patients with movement-related pain due to bone metastases. Clin J Pain 25: 648-649.
65. Riccio AI, Wodajo FM, Malawer M (2007) Metastatic carcinoma of the long bones. Am Fam Physician 76: 1489-1494.
66. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, et al. (2000) Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneu-rons: A novel neuronal marker of nerve injury. Mol Cell Neurosci 15: 170-182.
67. Obata K, Yamanaka H, Fukuoka T, Yi D, Tokunaga A, et al. (2003) Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain 101: 65-77.
68. Peters CM, Ghilardi JR, Keyser CP, Kubota K, Lindsay TH, et al. (2005) Tumor-induced injury of primary afferent sensory nerve fibers in bone cancer pain. Exp Neurol 193: 85-100.
69. Ghilardi JR, Rohrich H, Lindsay TH, Sevcik MA, Schwei MJ, et al. (2005) Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J Neurosci 25: 3126-3131.
70. Sevcik MA, Ghilardi JR, Peters CM, Lindsay TH, Halvorson KG, et al. (2005) Anti-NGF therapy profoundly reduces bone cancer pain and the accompanying increase in markers of peripheral and central sensitization. Pain 115: 128-141.
71. Honore P, Schwei J, Rogers SD, Salak-Johnson JL, Finke MP, et al. (2000) Cellular and neurochemical remodeling of the spinal cord in bone cancer pain. Progress in brain research 129: 389-397.
72. Dworkin RH (2002) An overview of neuropathic pain: syndromes, symptoms, signs, and several mechanisms. Clin J Pain 18: 343-349.
73. Romero-Sandoval A, Nutile-McMenemy N, DeLeo JA (2008) Spinal microglial and perivascular cell cannabinoid receptor type 2 activation reduces behavioral hypersensitivity without tolerance after peripheral nerve injury. Anesthesiology 108: 722-734.
74. Hald A, Nedergaard S, Hansen RR, Ding M, Heegaard AM (2009) Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Eur J Pain 13: 138-145.
75. Denes A, Boldogkoi Z, Uhereczky G, Hornyak A, Rusvai M, et al. (2005) Central autonomic control of the bone marrow: multisynaptic tract tracing by recombinant pseudorabies virus. Neuroscience 134: 947-963.
76. Scholz J, Woolf CJ (2007) The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368.
77. Schirrmeister H, Guhlmann A, Elsner K, Kotzerke J, Glatting G, et al. (1999) Sensitivity in detecting osseous lesions depends on anatomic localization: planar bone scintigraphy versus 18F PET. J Nucl Med 40: 1623-1629.
78. Muller-Horvat C, Radny P, Eigentler TK, Schafer J, Pfannenberg C, et al. (2006) Prospective comparison of the impact on treatment decisions of whole-body magnetic resonance imaging and computed tomography in patients with metastatic malignant melanoma. Eur J Cancer 42: 342-350.
79. Pichler BJ, Wehrl HF, Kolb A, Judenhofer MS (2008) Positron emission tomography/magnetic resonance imaging: the next generation of multimodality imaging? Semin Nucl Med 38: 199-208.
80. Kingsley LA, Fournier PG, Chirgwin JM, Guise TA (2007) Molecular biology of bone metastasis. Mol Cancer Ther 6: 2609-2617.
81. Rauch F (2009) Bone Biopsy: Indications and Methods. Endocr Dev 16: 49-57.
82. Armamento-Villareal R, Napoli N, Diemer K, Watkins M, Civitelli R, et al. (2009) Bone turnover in bone biopsies of patients with low-energy cortical fractures receiving bisphosphonates: a case series. Calcif Tissue Int 85: 37-44.
83. Hahn M, Vogel M, Pompesius-Kempa M, Delling G (1992) Trabecular bone pattern factor-a new parameter for simple quantification of bone microarchitecture. Bone 13: 327-330.
84. Halvorson KG, Sevcik MA, Ghilardi JR, Rosol TJ, Mantyh PW (2006) Similarities and differences in tumor growth, skeletal remodeling and pain in an osteolytic and osteoblastic model of bone cancer. Clin J Pain 22: 587-600.
85. Roodman GD, Dougall WC (2008) RANK ligand as a therapeutic target for bone metastases and multiple myeloma. Cancer Treat Rev 34: 92-101.