Effect of Long-time Mild Heat Stress on Proliferative, Differentiation and Bone Regeneration Capabilities of Dental Pulp Stem Cells
Regeneration, Reconstruction & Restoration (Triple R),
Vol. 6 (2021),
13 March 2021
,
Page e13
https://doi.org/10.22037/rrr.v6i.40431
Abstract
Introduction: The application of various strategies, including heat stress, has been attempted to maintain and improve mesenchymal stem cells (MSCs) plasticity and efficiency for bone regeneration. Although cell responses to heat stress are one of the most examined cellular stress responses, most studies, in this context, investigated the effect of that for a short period. Hence, the current study aimed to investigate the properties of MSCs, derived from dental pulp stem cells (DPSCs) following long-term heat stress.
Materials and Methods: DPSCs was loaded on β-tricalcium phosphate scaffold blocks and cultivated at elevated temperature up to 39 ° C. In vitro, DPSC properties, including proliferation, osteogenic differentiation, and bone regeneration in vivo, have been evaluated.
Results: The results of in vitro study showed that mild heat stress for a lengthy period could maintain and improve both the proliferative and differentiation potential of DPSCs during in vitro expansion and differentiation. Also, bone regeneration in vivo showed increased bone regeneration in the cells cultivated at a higher temperature.
Conclusion: This study provided evidence for the beneficial effects of the administration of mild heat stress for an extended period to maintain and improve DPSC properties, which may serve as a starting point for developing clinically compliant procedures for MSC treatment before transplantation.
Keywords:
- Bone regeneration
- Dental pulp stem cells
- Heat stress
How to Cite
Moslemi, H., Paknejad , Z. ., Farzad Mohajeri, S., & Khojasteh, A. . (2023). Effect of Long-time Mild Heat Stress on Proliferative, Differentiation and Bone Regeneration Capabilities of Dental Pulp Stem Cells. Regeneration, Reconstruction & Restoration (Triple R), 6, e13. https://doi.org/10.22037/rrr.v6i.40431
References
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11. Haider HK, Ashraf M. Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation. Journal of molecular and cellular cardiology. 2008;45(4):554-66.
12. Arai F, Suda T. Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Annals of the New York Academy of Sciences. 2007;1106:41-53.
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17. Yao S, Gutierrez DL, He H, Dai Y, Liu D, Wise GE. Proliferation of dental follicle-derived cell populations in heat-stress conditions. Cell proliferation. 2011;44(5):486-93.
18. Cmielova J, Havelek R, Soukup T, Jiroutova A, Visek B, Suchanek J, et al. Gamma radiation induces senescence in human adult mesenchymal stem cells from bone marrow and periodontal ligaments. International journal of radiation biology. 2012;88(5):393-404.
19. Dai Y, He H, Wise GE, Yao S. Hypoxia promotes growth of stem cells in dental follicle cell populations. Journal of biomedical science and engineering. 2011;4(6):454-61.
20. Iida K, Takeda-Kawaguchi T, Tezuka Y, Kunisada T, Shibata T, Tezuka K. Hypoxia enhances colony formation and proliferation but inhibits differentiation of human dental pulp cells. Archives of oral biology. 2010;55(9):648-54.
21. Kanafi M, Ramesh A, Gupta P, Bhonde R. Influence of hypoxia, high glucose, and low serum on the growth kinetics of mesenchymal stem cells from deciduous and permanent teeth. Cells Tissues Organs. 2013;198(3):198-208.
22. Sakdee JB, White RR, Pagonis TC, Hauschka PV. Hypoxia-amplified proliferation of human dental pulp cells. Journal of endodontics. 2009;35(6):818-23.
23. Vanacker J, Viswanath A, De Berdt P, Everard A, Cani PD, Bouzin C, et al. Hypoxia modulates the differentiation potential of stem cells of the apical papilla. Journal of endodontics. 2014;40(9):1410-8.
24. Zhou Y, Fan W, Xiao Y. The Effect of Hypoxia on the Stemness and Differentiation Capacity of PDLC and DPC. Biomed Res Int. 2014;2014:890675.
25. Stolzing A, Sethe S, Scutt AM. Stressed stem cells: Temperature response in aged mesenchymal stem cells. Stem cells and development. 2006;15(4):478-87.
26. Alekseenko LL, Zemelko VI, Domnina AP, Lyublinskaya OG, Zenin VV, Pugovkina NA, et al. Sublethal heat shock induces premature senescence rather than apoptosis in human mesenchymal stem cells. Cell stress & chaperones. 2014;19(3):355-66.
27. Andreeva NV, Zatsepina OG, Garbuz DG, Evgen'ev MB, Belyavsky AV. Recombinant HSP70 and mild heat shock stimulate growth of aged mesenchymal stem cells. Cell stress & chaperones. 2016;21(4):727-33.
28. Choudhery MS, Badowski M, Muise A, Harris DT. Effect of mild heat stress on the proliferative and differentiative ability of human mesenchymal stromal cells. Cytotherapy. 2015;17(4):359-68.
29. Lee MW, Muramatsu T, Uekusa T, Lee JH, Shimono M. Heat stress induces alkaline phosphatase activity and heat shock protein 25 expression in cultured pulp cells. International endodontic journal. 2008;41(2):158-62.
30. Norgaard R, Kassem M, Rattan SI. Heat shock-induced enhancement of osteoblastic differentiation of hTERT-immortalized mesenchymal stem cells. Annals of the New York Academy of Sciences. 2006;1067:443-7.
31. Rezai Rad M, Wise GE, Brooks H, Flanagan MB, Yao S. Activation of proliferation and differentiation of dental follicle stem cells (DFSCs) by heat stress. Cell proliferation. 2013;46(1):58-66.
32. Shui C, Scutt A. Mild heat shock induces proliferation, alkaline phosphatase activity, and mineralization in human bone marrow stromal cells and Mg-63 cells in vitro. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2001;16(4):731-41.
33. Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA, et al. Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PloS one. 2013;8(6):e64752.
34. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(19):8639-43.
35. Yamaguchi T, Suzuki T, Arai H, Tanabe S, Atomi Y. Continuous mild heat stress induces differentiation of mammalian myoblasts, shifting fiber type from fast to slow. American journal of physiology Cell physiology. 2010;298(1):C140-8.
36. Chen J, Shi ZD, Ji X, Morales J, Zhang J, Kaur N, et al. Enhanced osteogenesis of human mesenchymal stem cells by periodic heat shock in self-assembling peptide hydrogel. Tissue engineering Part A. 2013;19(5-6):716-28.
37. Fan GC. Role of heat shock proteins in stem cell behavior. Progress in molecular biology and translational science. 2012;111:305-22.
38. Khojasteh A, Nazeman P, Rad MR. Dental stem cells in oral, maxillofacial and craniofacial regeneration. Dental Stem Cells: Springer; 2016. p. 143-65.
39. Gregory CA, Gunn WG, Peister A, Prockop DJ. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Analytical biochemistry. 2004;329(1):77-84.
40. Khojasteh A, Behnia H, Naghdi N, Esmaeelinejad M, Alikhassy Z, Stevens M. Effects of different growth factors and carriers on bone regeneration: a systematic review. Oral surgery, oral medicine, oral pathology and oral radiology. 2013;116(6):e405-23.
41. Aravamudhan A, Ramos DM, Nip J, Subramanian A, James R, Harmon MD, et al. Osteoinductive small molecules: growth factor alternatives for bone tissue engineering. Current pharmaceutical design. 2013;19(19):3420-8.
42. Calabrese V, Cornelius C, Dinkova-Kostova AT, Iavicoli I, Di Paola R, Koverech A, et al. Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochimica et biophysica acta. 2012;1822(5):753-83.
43. Alekseenko LL, Zemelko VI, Zenin VV, Pugovkina NA, Kozhukharova IV, Kovaleva ZV, et al. Heat shock induces apoptosis in human embryonic stem cells but a premature senescence phenotype in their differentiated progeny. Cell Cycle. 2012;11(17):3260-9.
44. Richards V, Stofer R. The stimulation of bone growth by internal heating. Surgery. 1959;46(1):84-96.
45. Doyle JR, Smart BW. Stimulation of bone growth by short-wave diathermy. JBJS. 1963;45(1):15-24.
46. Brookes M, May KU. The influence of temperature on bone growth in the chick. Journal of Anatomy. 1972;111(Pt 3):351-63.
47. Weinberger A, Abramonvici A, Fadila R, Levy A, Giler S, Lev A. The effect of local deep microwave hyperthermia on experimental zymosan-induced arthritis in rabbits. American journal of physical medicine & rehabilitation. 1990;69(5):239-44.
48. Zambito A, Campacci R, Olivati N, Rossi F, Spagnol G, Fraccaroli G. [Rehabilitative approach in osteoarticular pathology in the elderly]. Minerva medica. 1986;77(32-33):1501-6.
49. Carter DL, MacFall JR, Clegg ST, Wan X, Prescott DM, Charles HC, et al. Magnetic resonance thermometry during hyperthermia for human high-grade sarcoma. International journal of radiation oncology, biology, physics. 1998;40(4):815-22.
50. Akagi M, Tsuboyama T, Ikenaga M, Matsusue Y, Hiraoka M, Nakamura T. Anti-tumour effects of localized hyperthermia on an experimental bone tumour using an intramedullary nail. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1997;13(4):387-400.
51. Fan QY, Ma BA, Qlu XC, Li YL, Ye J, Zhou Y. Preliminary report on treatment of bone tumors with microwave-induced hyperthermia. Bioelectromagnetics. 1996;17(3):218-22.
52. Wiedemann GJ, d'Oleire F, Knop E, Eleftheriadis S, Bucsky P, Feddersen S, et al. Ifosfamide and carboplatin combined with 41.8 degrees C whole-body hyperthermia in patients with refractory sarcoma and malignant teratoma. Cancer research. 1994;54(20):5346-50.
53. Tsukiyama I, Ogino T, Egawa S. Hyperthermia for bone and soft tissue sarcoma: relationship between computerized tomographic and histological findings. Radiation medicine. 1994;12(5):231-6.
54. Ikenaga M, Ohura K, Kotoura Y, Yamamuro T, Nakamura T, Oka M, et al. Hyperthermic treatment of canine tibia through RF inductive heating of an intramedullary nail: a new experimental approach to hyperthermia for metastatic bone tumours. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1994;10(4):507-16.
55. Ogawa H. [Effects of the localized thermal enhancement on new bone formation following mechanical expansion of the rat sagittal suture]. Nihon Kyosei Shika Gakkai zasshi = The journal of Japan Orthodontic Society. 1990;49(6):485-96.
56. Leon SA, Asbell SO, Arastu HH, Edelstein G, Packel AJ, Sheehan S, et al. Effects of hyperthermia on bone. II. Heating of bone in vivo and stimulation of bone growth. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1993;9(1):77-87.
2. Khojasteh A, Sadeghi N. Application of buccal fat pad-derived stem cells in combination with autogenous iliac bone graft in the treatment of maxillomandibular atrophy: a preliminary human study. International journal of oral and maxillofacial surgery. 2016;45(7):864-71.
3. Behnia H, Khojasteh A, Soleimani M, Tehranchi A, Atashi A. Repair of alveolar cleft defect with mesenchymal stem cells and platelet derived growth factors: a preliminary report. Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery. 2012;40(1):2-7.
4. Shayesteh YS, Khojasteh A, Soleimani M, Alikhasi M, Khoshzaban A, Ahmadbeigi N. Sinus augmentation using human mesenchymal stem cells loaded into a beta-tricalcium phosphate/hydroxyapatite scaffold. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2008;106(2):203-9.
5. Behnia H, Khojasteh A, Soleimani M, Tehranchi A, Khoshzaban A, Keshel SH, et al. Secondary repair of alveolar clefts using human mesenchymal stem cells. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2009;108(2):e1-6.
6. Wall ME, Bernacki SH, Loboa EG. Effects of serial passaging on the adipogenic and osteogenic differentiation potential of adipose-derived human mesenchymal stem cells. Tissue engineering. 2007;13(6):1291-8.
7. Bonab MM, Alimoghaddam K, Talebian F, Ghaffari SH, Ghavamzadeh A, Nikbin B. Aging of mesenchymal stem cell in vitro. BMC cell biology. 2006;7:14.
8. Rezai Rad M, Bova JF, Orooji M, Pepping J, Qureshi A, Piero FD, et al. Evaluation of bone regeneration potential of dental follicle stem cells (DFSCs) for treatment of craniofacial defects. Cytotherapy. 2015.
9. Haider H, Ashraf M. Bone marrow cell transplantation in clinical perspective. Journal of molecular and cellular cardiology. 2005;38(2):225-35.
10. Pasha Z, Wang Y, Sheikh R, Zhang D, Zhao T, Ashraf M. Preconditioning enhances cell survival and differentiation of stem cells during transplantation in infarcted myocardium. Cardiovascular research. 2008;77(1):134-42.
11. Haider HK, Ashraf M. Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation. Journal of molecular and cellular cardiology. 2008;45(4):554-66.
12. Arai F, Suda T. Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Annals of the New York Academy of Sciences. 2007;1106:41-53.
13. Orford KW, Scadden DT. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nature reviews Genetics. 2008;9(2):115-28.
14. Park Y, Gerson SL. DNA repair defects in stem cell function and aging. Annual review of medicine. 2005;56:495-508.
15. Wang YZ, Plane JM, Jiang P, Zhou CJ, Deng W. Concise review: Quiescent and active states of endogenous adult neural stem cells: identification and characterization. Stem cells (Dayton, Ohio). 2011;29(6):907-12.
16. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-29.
17. Yao S, Gutierrez DL, He H, Dai Y, Liu D, Wise GE. Proliferation of dental follicle-derived cell populations in heat-stress conditions. Cell proliferation. 2011;44(5):486-93.
18. Cmielova J, Havelek R, Soukup T, Jiroutova A, Visek B, Suchanek J, et al. Gamma radiation induces senescence in human adult mesenchymal stem cells from bone marrow and periodontal ligaments. International journal of radiation biology. 2012;88(5):393-404.
19. Dai Y, He H, Wise GE, Yao S. Hypoxia promotes growth of stem cells in dental follicle cell populations. Journal of biomedical science and engineering. 2011;4(6):454-61.
20. Iida K, Takeda-Kawaguchi T, Tezuka Y, Kunisada T, Shibata T, Tezuka K. Hypoxia enhances colony formation and proliferation but inhibits differentiation of human dental pulp cells. Archives of oral biology. 2010;55(9):648-54.
21. Kanafi M, Ramesh A, Gupta P, Bhonde R. Influence of hypoxia, high glucose, and low serum on the growth kinetics of mesenchymal stem cells from deciduous and permanent teeth. Cells Tissues Organs. 2013;198(3):198-208.
22. Sakdee JB, White RR, Pagonis TC, Hauschka PV. Hypoxia-amplified proliferation of human dental pulp cells. Journal of endodontics. 2009;35(6):818-23.
23. Vanacker J, Viswanath A, De Berdt P, Everard A, Cani PD, Bouzin C, et al. Hypoxia modulates the differentiation potential of stem cells of the apical papilla. Journal of endodontics. 2014;40(9):1410-8.
24. Zhou Y, Fan W, Xiao Y. The Effect of Hypoxia on the Stemness and Differentiation Capacity of PDLC and DPC. Biomed Res Int. 2014;2014:890675.
25. Stolzing A, Sethe S, Scutt AM. Stressed stem cells: Temperature response in aged mesenchymal stem cells. Stem cells and development. 2006;15(4):478-87.
26. Alekseenko LL, Zemelko VI, Domnina AP, Lyublinskaya OG, Zenin VV, Pugovkina NA, et al. Sublethal heat shock induces premature senescence rather than apoptosis in human mesenchymal stem cells. Cell stress & chaperones. 2014;19(3):355-66.
27. Andreeva NV, Zatsepina OG, Garbuz DG, Evgen'ev MB, Belyavsky AV. Recombinant HSP70 and mild heat shock stimulate growth of aged mesenchymal stem cells. Cell stress & chaperones. 2016;21(4):727-33.
28. Choudhery MS, Badowski M, Muise A, Harris DT. Effect of mild heat stress on the proliferative and differentiative ability of human mesenchymal stromal cells. Cytotherapy. 2015;17(4):359-68.
29. Lee MW, Muramatsu T, Uekusa T, Lee JH, Shimono M. Heat stress induces alkaline phosphatase activity and heat shock protein 25 expression in cultured pulp cells. International endodontic journal. 2008;41(2):158-62.
30. Norgaard R, Kassem M, Rattan SI. Heat shock-induced enhancement of osteoblastic differentiation of hTERT-immortalized mesenchymal stem cells. Annals of the New York Academy of Sciences. 2006;1067:443-7.
31. Rezai Rad M, Wise GE, Brooks H, Flanagan MB, Yao S. Activation of proliferation and differentiation of dental follicle stem cells (DFSCs) by heat stress. Cell proliferation. 2013;46(1):58-66.
32. Shui C, Scutt A. Mild heat shock induces proliferation, alkaline phosphatase activity, and mineralization in human bone marrow stromal cells and Mg-63 cells in vitro. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2001;16(4):731-41.
33. Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA, et al. Awakened by cellular stress: isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PloS one. 2013;8(6):e64752.
34. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(19):8639-43.
35. Yamaguchi T, Suzuki T, Arai H, Tanabe S, Atomi Y. Continuous mild heat stress induces differentiation of mammalian myoblasts, shifting fiber type from fast to slow. American journal of physiology Cell physiology. 2010;298(1):C140-8.
36. Chen J, Shi ZD, Ji X, Morales J, Zhang J, Kaur N, et al. Enhanced osteogenesis of human mesenchymal stem cells by periodic heat shock in self-assembling peptide hydrogel. Tissue engineering Part A. 2013;19(5-6):716-28.
37. Fan GC. Role of heat shock proteins in stem cell behavior. Progress in molecular biology and translational science. 2012;111:305-22.
38. Khojasteh A, Nazeman P, Rad MR. Dental stem cells in oral, maxillofacial and craniofacial regeneration. Dental Stem Cells: Springer; 2016. p. 143-65.
39. Gregory CA, Gunn WG, Peister A, Prockop DJ. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Analytical biochemistry. 2004;329(1):77-84.
40. Khojasteh A, Behnia H, Naghdi N, Esmaeelinejad M, Alikhassy Z, Stevens M. Effects of different growth factors and carriers on bone regeneration: a systematic review. Oral surgery, oral medicine, oral pathology and oral radiology. 2013;116(6):e405-23.
41. Aravamudhan A, Ramos DM, Nip J, Subramanian A, James R, Harmon MD, et al. Osteoinductive small molecules: growth factor alternatives for bone tissue engineering. Current pharmaceutical design. 2013;19(19):3420-8.
42. Calabrese V, Cornelius C, Dinkova-Kostova AT, Iavicoli I, Di Paola R, Koverech A, et al. Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity. Biochimica et biophysica acta. 2012;1822(5):753-83.
43. Alekseenko LL, Zemelko VI, Zenin VV, Pugovkina NA, Kozhukharova IV, Kovaleva ZV, et al. Heat shock induces apoptosis in human embryonic stem cells but a premature senescence phenotype in their differentiated progeny. Cell Cycle. 2012;11(17):3260-9.
44. Richards V, Stofer R. The stimulation of bone growth by internal heating. Surgery. 1959;46(1):84-96.
45. Doyle JR, Smart BW. Stimulation of bone growth by short-wave diathermy. JBJS. 1963;45(1):15-24.
46. Brookes M, May KU. The influence of temperature on bone growth in the chick. Journal of Anatomy. 1972;111(Pt 3):351-63.
47. Weinberger A, Abramonvici A, Fadila R, Levy A, Giler S, Lev A. The effect of local deep microwave hyperthermia on experimental zymosan-induced arthritis in rabbits. American journal of physical medicine & rehabilitation. 1990;69(5):239-44.
48. Zambito A, Campacci R, Olivati N, Rossi F, Spagnol G, Fraccaroli G. [Rehabilitative approach in osteoarticular pathology in the elderly]. Minerva medica. 1986;77(32-33):1501-6.
49. Carter DL, MacFall JR, Clegg ST, Wan X, Prescott DM, Charles HC, et al. Magnetic resonance thermometry during hyperthermia for human high-grade sarcoma. International journal of radiation oncology, biology, physics. 1998;40(4):815-22.
50. Akagi M, Tsuboyama T, Ikenaga M, Matsusue Y, Hiraoka M, Nakamura T. Anti-tumour effects of localized hyperthermia on an experimental bone tumour using an intramedullary nail. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1997;13(4):387-400.
51. Fan QY, Ma BA, Qlu XC, Li YL, Ye J, Zhou Y. Preliminary report on treatment of bone tumors with microwave-induced hyperthermia. Bioelectromagnetics. 1996;17(3):218-22.
52. Wiedemann GJ, d'Oleire F, Knop E, Eleftheriadis S, Bucsky P, Feddersen S, et al. Ifosfamide and carboplatin combined with 41.8 degrees C whole-body hyperthermia in patients with refractory sarcoma and malignant teratoma. Cancer research. 1994;54(20):5346-50.
53. Tsukiyama I, Ogino T, Egawa S. Hyperthermia for bone and soft tissue sarcoma: relationship between computerized tomographic and histological findings. Radiation medicine. 1994;12(5):231-6.
54. Ikenaga M, Ohura K, Kotoura Y, Yamamuro T, Nakamura T, Oka M, et al. Hyperthermic treatment of canine tibia through RF inductive heating of an intramedullary nail: a new experimental approach to hyperthermia for metastatic bone tumours. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1994;10(4):507-16.
55. Ogawa H. [Effects of the localized thermal enhancement on new bone formation following mechanical expansion of the rat sagittal suture]. Nihon Kyosei Shika Gakkai zasshi = The journal of Japan Orthodontic Society. 1990;49(6):485-96.
56. Leon SA, Asbell SO, Arastu HH, Edelstein G, Packel AJ, Sheehan S, et al. Effects of hyperthermia on bone. II. Heating of bone in vivo and stimulation of bone growth. International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group. 1993;9(1):77-87.
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