Volume 126, Issue 10 pp. E325-E331

Laryngology

Biomechanical and biochemical characterization of porcine tracheal cartilage

Benjamin Hoffman BS,

Benjamin Hoffman BS

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

Search for more papers by this author

Matthew Martin BS,

Matthew Martin BS

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

Search for more papers by this author

Bryan N. Brown PhD,

Bryan N. Brown PhD

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A

Search for more papers by this author

Lawrence J. Bonassar PhD,

Lawrence J. Bonassar PhD

Department of Biomedical Engineering, Cornell University, Ithaca, New York

Search for more papers by this author

Jonathan Cheetham VetMB, PhD, DACVS,

Corresponding Author

Jonathan Cheetham VetMB, PhD, DACVS

[email protected]

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A

Send correspondence to Jonathan Cheetham, VetMB, PhD, DACVS, Department of Clinical Sciences, College of Veterinary Medicine, Ithaca, NY, 14850. E-Mail: [email protected]Search for more papers by this author

Benjamin Hoffman BS,

Benjamin Hoffman BS

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

Search for more papers by this author

Matthew Martin BS,

Matthew Martin BS

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

Search for more papers by this author

Bryan N. Brown PhD,

Bryan N. Brown PhD

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A

Search for more papers by this author

Lawrence J. Bonassar PhD,

Lawrence J. Bonassar PhD

Department of Biomedical Engineering, Cornell University, Ithaca, New York

Search for more papers by this author

Jonathan Cheetham VetMB, PhD, DACVS,

Corresponding Author

Jonathan Cheetham VetMB, PhD, DACVS

[email protected]

Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York

McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, U.S.A

First published: 30 January 2016

https://doi.org/10.1002/lary.25861

Citations: 20

The authors have no funding, financial relationships, or conflicts of interest to disclose.

Share a link

Email
Wechat
Bluesky

Abstract

Objectives/Hypothesis

The trachea is essential to respiratory function and is a mechanically and biochemically complex composite tissue. Tissue-engineering approaches to treat tracheal diseases require detailed knowledge of the native mechanical and biochemical properties of the trachea. Although the porcine trachea represents an excellent preclinical model, relevant mechanical and biochemical composition are incompletely characterized.

Study Design

Experimental. The mechanical and biochemical properties of 12 intact porcine tracheas were determined to characterize their compliance, as well as the aggregate modulus, bidirectional elastic modulus, hydraulic permeability, and biochemical characteristics of individual cartilage rings.

Results

Data demonstrate the glycosaminoglycan content of tracheal rings was (mean ± standard deviation) 190 ± 49 μg/mg. Hydroxyproline content was 8.2 ± 3.2 μg/mg, and DNA content was 1.3 ± 0.27 μg/mg, a four-fold difference between circumferential elastic modulus (5.6 ± 2.0 megapascal [MPa]) and longitudinal composite elastic modulus (1.1 ± 0.7 MPa, P < 0.0001) was also observed. Aggregate modulus (stiffness) of porcine tracheal rings was 1.30 ± 0.28 MPa, and inflationary compliance was 0.00472 ± 0.00188 cmH₂O⁻¹.

Conclusion

This study presents a comprehensive characterization of the relevant biochemical and mechanical properties of porcine tracheal cartilage, which is considered an excellent candidate for xenogenic tracheal graft and a source for tissue-engineered tracheal reconstruction. The range of parameters characterized in this study agrees with those reported for hyaline cartilage of the airway in other species. These characteristics can be used as quantitative benchmarks for tissue-engineering approaches to treat tracheal disease.

Level of Evidence

NA. Laryngoscope, 126:E325–E331, 2016

BIBLIOGRAPHY

1Wain JC. Postintubation tracheal stenosis. Chest Surg Clin N Am 2003; 13: 231–246.
10.1016/S1052-3359(03)00034-6
PubMed Google Scholar
2Zias N, Chroneou A, Tabba MK, et al. Post tracheostomy and post intubation tracheal stenosis: report of 31 cases and review of the literature. BMC Pulm Med 2008; 8: 18.
10.1186/1471-2466-8-18
PubMed Google Scholar
3Grillo HC. Tracheal replacement: a critical review. Ann Thorac Surg 2002; 73: 1995–2004.
10.1016/S0003-4975(02)03564-6
PubMed Web of Science® Google Scholar
4Chao MW, Smith JG, Laidlaw C, Joon DL, Ball D. Results of treating primary tumors of the trachea with radiotherapy. Int J Radiat Oncol Biol Phys 1998; 41: 779–785.
10.1016/S0360-3016(98)00120-5
CAS PubMed Web of Science® Google Scholar
5Manninen MP, Pukander JS, Flander MK, Laippala PJ, Huhtala HS, Karma PH. Treatment of primary tracheal carcinoma in Finland in 1967–1985. Acta Oncol 1993; 32: 277–282.
10.3109/02841869309093595
CAS PubMed Web of Science® Google Scholar
6Baiguera S, Birchall MA, Macchiarini P. Tissue-engineered tracheal transplantation. Transplantation 2010; 89: 485–491.
10.1097/TP.0b013e3181cd4ad3
PubMed Web of Science® Google Scholar
7Orlando G, Baptista P, Birchall M, et al. Regenerative medicine as applied to solid organ transplantation: current status and future challenges. Transpl Int 2011; 24: 223–232.
10.1111/j.1432-2277.2010.01182.x
PubMed Google Scholar
8Nakamura T, Ohmori K, Kanemaru S. Tissue-engineered airway and “in situ tissue engineering”. Gen Thorac Cardiovasc Surg 2011; 59: 91–97.
10.1007/s11748-010-0677-9
PubMed Google Scholar
9Macchiarini P, Jungebluth P, Go T, et al. Clinical transplantation of a tissue-engineered airway. Lancet 2008; 372: 2023–2030.
10.1016/S0140-6736(08)61598-6
PubMed Web of Science® Google Scholar
10Badylak SF, Weiss DJ, Caplan A, Macchiarini P. Engineered whole organs and complex tissues. Lancet 2012; 379: 943–952.
10.1016/S0140-6736(12)60073-7
PubMed Web of Science® Google Scholar
11ten Hallers EJ, Rakhorst G, Marres HA, et al. Animal models for tracheal research. Biomaterials 2004; 25: 1533–1543.
10.1016/S0142-9612(03)00500-3
CAS PubMed Web of Science® Google Scholar
12Peretti GM, Xu JW, Bonassar LJ, Kirchhoff CH, Yaremchuk MJ, Randolph MA. Review of injectable cartilage engineering using fibrin gel in mice and swine models. Tissue Eng 2006; 12: 1151–1168.
10.1089/ten.2006.12.1151
CAS PubMed Web of Science® Google Scholar
13Ballyns JJ, Wright TM, Bonassar LJ. Effect of media mixing on ECM assembly and mechanical properties of anatomically-shaped tissue engineered meniscus. Biomaterials 2010; 31: 6756–6763.
10.1016/j.biomaterials.2010.05.039
CAS PubMed Web of Science® Google Scholar
14Bowles RD, Williams RM, Zipfel WR, Bonassar LJ. Self-assembly of aligned tissue-engineered annulus fibrosus and intervertebral disc composite via collagen gel contraction. Tissue Eng Part A 2010; 16: 1339–1348.
10.1089/ten.tea.2009.0442
CAS PubMed Web of Science® Google Scholar
15Mizuno H, Roy AK, Zaporojan V, Vacanti CA, Ueda M, Bonassar LJ. Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials 2006; 27: 362–370.
10.1016/j.biomaterials.2005.06.042
CAS PubMed Web of Science® Google Scholar
16Weinand C, Peretti GM, Adams SB Jr, Bonassar LJ, Randolph MA, Gill TJ. An allogenic cell-based implant for meniscal lesions. Am J Sports Med 2006; 34: 1779–1789.
10.1177/0363546506290666
PubMed Web of Science® Google Scholar
17Brown BN, Siebenlist NJ, Cheetham J, Ducharme NG, Rawlinson JJ, Bonassar LJ. Tissue Engineering Part C: Methods. 2014; 20: 506–513.
Google Scholar
18Badylak SF. The extracellular matrix as a biologic scaffold material. Biomaterials 2007; 28: 3587–3593.
10.1016/j.biomaterials.2007.04.043
CAS PubMed Web of Science® Google Scholar
19Roberts CR, Rains JK, Pare PD, Walker DC, Wiggs B, Bert JL. Ultrastructure and tensile properties of human tracheal cartilage. J Biomech 1998; 31: 81–86.
10.1016/S0021-9290(97)00112-7
CAS PubMed Web of Science® Google Scholar
20Rains JK, Bert JL, Roberts CR, Pare PD. Mechanical properties of human tracheal cartilage. J Appl Physiol (1985) 1992; 72: 219–225.
10.1152/jappl.1992.72.1.219
CAS PubMed Web of Science® Google Scholar
21Croteau JR, Cook CD. Volume-pressure and length-tension measurements in human tracheal and bronchial segments. J Appl Physiol 1961; 16: 170–172.
10.1152/jappl.1961.16.1.170
CAS PubMed Web of Science® Google Scholar
22Winter DC. Elastic properties of collapsing and expanding trachea. J Biomech Eng 1985; 107: 300–303.
10.1115/1.3138559
CAS PubMed Web of Science® Google Scholar
23Coburn RF, Palombini B. Time-dependent pressure-volume relationships of the in vivo canine trachea. Respir Physiol 1972; 16: 282–289.
10.1016/0034-5687(72)90058-8
CAS PubMed Web of Science® Google Scholar
24Coppit G, Perkins J, Munaretto J, Nielsen R, McKinney L, Ulnick K. The effects of mitomycin-C and stenting on airway wound healing after laryngotracheal reconstruction in a pig model. Int J Pediatr Otorhinolaryngol 2000; 53: 125–135.
10.1016/S0165-5876(00)00322-0
CAS PubMed Web of Science® Google Scholar
25Barker E, Murison P, Macchiarini P, et al. Early immunological changes associated with laryngeal transplantation in a major histocompatibility complex-matched pig model. Clin Exp Immunol 2006; 146: 503–508.
10.1111/j.1365-2249.2006.03232.x
CAS PubMed Web of Science® Google Scholar
26Murison PJ, Jones A, Mitchard L, Burt R, Birchall MA. Development of perioperative care for pigs undergoing laryngeal transplantation: a case series. Lab Anim 2009; 43: 338–343.
10.1258/la.2009.008101
CAS PubMed Web of Science® Google Scholar
27Jungebluth P, Go T, Asnaghi A, et al. Structural and morphologic evaluation of a novel detergent-enzymatic tissue-engineered tracheal tubular matrix. J Thorac Cardiovasc Surg 2009; 138: 586–593; discussion 592–593.
10.1016/j.jtcvs.2008.09.085
CAS PubMed Web of Science® Google Scholar
28Go T, Jungebluth P, Baiguera S, et al. Both epithelial cells and mesenchymal stem cell-derived chondrocytes contribute to the survival of tissue-engineered airway transplants in pigs. J Thorac Cardiovasc Surg 2010; 139: 437–443.
10.1016/j.jtcvs.2009.10.002
CAS PubMed Web of Science® Google Scholar
29Faulkner JA, Mair EA. Growth and development of homograft tracheal transplants in the piglet model. Arch Otolaryngol Head Neck Surg 2001; 127: 426–431.
10.1001/archotol.127.4.426
CAS PubMed Web of Science® Google Scholar
30Macchiarini P, Lenot B, de Montpreville V, et al. Heterotopic pig model for direct revascularization and venous drainage of tracheal allografts. Paris-Sud University Lung Transplantation Group. J Thorac Cardiovasc Surg 1994; 108: 1066–1075.
10.1016/S0022-5223(94)70149-0
CAS PubMed Web of Science® Google Scholar
31Changoor A, Fereydoonzad L, Yaroshinsky A, Buschmann MD. Effects of refrigeration and freezing on the electromechanical and biomechanical properties of articular cartilage. J Biomech Eng 2010; 132: 064502.
10.1115/1.4000991
PubMed Web of Science® Google Scholar
32Szarko M, Muldrew K, Bertram JE. Freeze-thaw treatment effects on the dynamic mechanical properties of articular cartilage. BMC Musculoskelet Disord 2010; 11: 231. doi: 10.1186/1471-2474-11-231.
10.1186/1471‐2474‐11‐231
PubMed Web of Science® Google Scholar
33Nonaka PN, Campillo N, Uriarte JJ, et al. Effects of freezing/thawing on the mechanical properties of decellularized lungs. J Biomed Mater Res A 2014; 102: 413–419.
10.1002/jbm.a.34708
CAS PubMed Web of Science® Google Scholar
34Remlinger NT, Czajka CA, Juhas ME, et al. Hydrated xenogeneic decellularized tracheal matrix as a scaffold for tracheal reconstruction. Biomaterials 2010; 31: 3520–3526.
10.1016/j.biomaterials.2010.01.067
CAS PubMed Web of Science® Google Scholar
35Teng Z, Wang Y, Li F, Yan H, Liu Z. Tracheal compliance and limit flow rate changes in a murine model of asthma. Sci China C Life Sci 2008; 51: 922–931.
10.1007/s11427-008-0108-7
PubMed Web of Science® Google Scholar
36Teng Z, Ochoa I, Li Z, Liao Z, Lin Y, Doblare M. Study on tracheal collapsibility, compliance, and stress by considering nonlinear mechanical property of cartilage. Ann Biomed Eng 2009; 37: 2380–2389.
10.1007/s10439-009-9765-3
PubMed Web of Science® Google Scholar
37Passman SN, Cheetham J, Bonassar LJ, Ducharme NG, Rawlinson J. Biomechanical characterisation of equine laryngeal cartilage. Equine Vet J 2011; 43: 592–598.
10.1111/j.2042-3306.2010.00315.x
CAS PubMed Web of Science® Google Scholar
38Mow VC, Kuei SC, Lai WM, Armstrong CG. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J Biomech Eng 1980; 102: 73–84.
10.1115/1.3138202
CAS PubMed Web of Science® Google Scholar
39Roy R, Boskey A, Bonassar LJ. Processing of type I collagen gels using nonenzymatic glycation. J Biomed Mater Res A 2010; 93: 843–851.
PubMed Web of Science® Google Scholar
40Kojima K, Bonassar LJ, Ignotz RA, Syed K, Cortiella J, Vacanti CA. Comparison of tracheal and nasal chondrocytes for tissue engineering of the trachea. Ann Thorac Surg 2003; 76: 1884–1888.
10.1016/S0003-4975(03)01193-7
PubMed Web of Science® Google Scholar
41Drury JL, Dennis RG, Mooney DJ. The tensile properties of alginate hydrogels. Biomaterials 2004; 25: 3187–3199.
10.1016/j.biomaterials.2003.10.002
CAS PubMed Web of Science® Google Scholar
42Enobakhare BO, Bader DL, Lee DA. Quantification of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue. Anal Biochem 1996; 243: 189–191.
10.1006/abio.1996.0502
CAS PubMed Web of Science® Google Scholar
43Neuman RE, Logan MA. The determination of hydroxyproline. J Biol Chem 1950; 184: 299–306.
10.1016/S0021-9258(19)51149-8
CAS PubMed Web of Science® Google Scholar
44Kim YJ, Sah RL, Doong JY, Grodzinsky AJ. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 1988; 174: 168–176.
10.1016/0003-2697(88)90532-5
CAS PubMed Web of Science® Google Scholar
45Rotter N, Tobias G, Lebl M, et al. Age-related changes in the composition and mechanical properties of human nasal cartilage. Arch Biochem Biophys 2002; 403: 132–140.
10.1016/S0003-9861(02)00263-1
CAS PubMed Web of Science® Google Scholar
46Breatnach E, Abbott GC, Fraser RG. Dimensions of the normal human trachea. AJR Am J Roentgenol 1984; 142: 903–906.
10.2214/ajr.142.5.903
CAS PubMed Web of Science® Google Scholar
47Costantino ML, Bagnoli P, Dini G, et al. A numerical and experimental study of compliance and collapsibility of preterm lamb tracheae. J Biomech 2004; 37: 1837–1847.
10.1016/j.jbiomech.2004.02.035
CAS PubMed Web of Science® Google Scholar
48Kojima K, Bonassar LJ, Roy AK, Mizuno H, Cortiella J, Vacanti CA. A composite tissue-engineered trachea using sheep nasal chondrocyte and epithelial cells. FASEB J 2003; 17: 823–828.
10.1096/fj.02-0462com
CAS PubMed Web of Science® Google Scholar
49Penn RB, Wolfson MR, Shaffer TH. Effect of ventilation on mechanical properties and pressure-flow relationships of immature airways. Pediatr Res 1988; 23: 519–524.
10.1203/00006450-198805000-00017
CAS PubMed Web of Science® Google Scholar
50Dabanoglu I, Ocal MK, Kara ME. A quantitative study on the trachea of the dog. Anat Histol Embryol 2001; 30: 57–59.
10.1046/j.1439-0264.2001.00301.x
CAS PubMed Web of Science® Google Scholar
51Martin HB, Proctor DF. Pressure-volume measurements on dog bronchi. J Appl Physiol 1958; 13: 337–343.
CAS PubMed Web of Science® Google Scholar
52Art T, Lekeux P. Mechanical properties of the isolated equine trachea. Res Vet Sci 1991; 51: 55–60.
10.1016/0034-5288(91)90031-I
CAS PubMed Web of Science® Google Scholar
53de Freitas RR, Pogliani FC, Moretti N Jr, et al. Tracheal morphometrics in the thoroughbred horse. Journal of Equine Veterinary Science 2001; 21: 240–243.
10.1016/S0737-0806(01)70043-3
Google Scholar
54Jones MC, Rueggeberg FA, Faircloth HA, et al. Defining the biomechanical properties of the rabbit trachea. Laryngoscope 2014; 124: 2352–2358. doi: 10.1002/lary.24739.
10.1002/lary.24739
PubMed Web of Science® Google Scholar

Citing Literature

Volume126, Issue10

October 2016

Pages E325-E331

Biomechanical and biochemical characterization of porcine tracheal cartilage

Abstract

Objectives/Hypothesis

Study Design

Results

Conclusion

Level of Evidence

BIBLIOGRAPHY

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Biomechanical and biochemical characterization of porcine tracheal cartilage

Abstract

Objectives/Hypothesis

Study Design

Results

Conclusion

Level of Evidence

BIBLIOGRAPHY

Citing Literature

References

Related

Information