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Annals of Biomedical Engineering

, Volume 40, Issue 10, pp 2255–2265 | Cite as

Stress State and Strain Rate Dependence of the Human Placenta

  • Benjamin C. Weed
  • Ali Borazjani
  • Sourav S. Patnaik
  • R. Prabhu
  • M. F. Horstemeyer
  • Peter L. Ryan
  • Thomas Franz
  • Lakiesha N. Williams
  • Jun Liao
Article

Abstract

Maternal trauma (MT) in automotive collisions is a source of injury, morbidity, and mortality for both mothers and fetuses. The primary associated pathology is placental abruption in which the placenta detaches from the uterus leading to hemorrhaging and termination of pregnancy. In this study, we focused on the differences in placental tissue response to different stress states (tension, compression, and shear) and different strain rates. Human placentas were obtained (n = 11) for mechanical testing and microstructure analysis. Specimens (n = 4+) were tested in compression, tension, and shear, each at three strain rates (nine testing protocols). Microstructure analysis included scanning electron microscopy, histology, and interrupted mechanical tests to observe tissue response to various loading states. Our data showed the greatest stiffness in tension, followed by compression, and then by shear. The study concludes that mechanical behavior of human placenta tissue (i) has a strong stress state dependence and (ii) behaves in a rate dependent manner in all three stress states, which had previously only been shown in tension. Interrupted mechanical tests revealed differences in the morphological microstructure evolution that was driven by the kinematic constraints from the different loading states. Furthermore, these structure–property data can be used to develop high fidelity constitutive models for MT simulations.

Keywords

Human placenta biomechanics Stress state dependence Strain rate dependence Maternal traumatic injury Placental abruption 

Notes

Acknowledgments

This study is supported by the MAFES SRI (awarded to JL) and Health Resources and Services Administration (HRSA) (DHHS R1CRH10429-01-00). We thank Karen Tiffen, RNC, Chrissy Poole, RNC, Dana Brooks, RNC, Cindy Patton, RN, Heather McMillian, ST, Bella Oswalt, ST, Sonya Anderson, RN, Rene Guines, ST, and other staff members of the Labor & Delivery Unit at OCH Regional Medical Center for their assistance with patient eligibility and tissue procurement; we also appreciate help from Amanda Lawrence (MSU EM Center) for her assistance in SEM imaging. We would also like to thank the Center for Advanced Vehicular Systems (CAVS) at the Mississippi State University for helping to support this research effort.

References

  1. 1.
    Abbassi-Ghanavati, M., B. M. Casey, C. Y. Spong, D. D. McIntire, L. M. Halvorson, and F. G. Cunningham. Pregnancy outcomes in women with thyroid peroxidase antibodies. Obstet. Gynecol. 116:381–386, 2010.PubMedCrossRefGoogle Scholar
  2. 2.
    Aboutanos, M. B. M. D. M. P. H., S. Z. M. D. Aboutanos, D. B. S. Dompkowski, T. M. M. D. Duane, A. K. M. D. Malhotra, and R. R. M. D. Ivatury. Significance of motor vehicle crashes and pelvic injury on fetal mortality: a five-year institutional review. J. Trauma-Inj. Infect. Crit. Care 65:616–620, 2008.CrossRefGoogle Scholar
  3. 3.
    Ananth, C. V., Y. Oyelese, L. Yeo, A. Pradhan, and A. M. Vintzileos. Placental abruption in the united states, 1979 through 2001: temporal trends and potential determinants. Am. J. Obstet. Gynecol. 192:191–198, 2005.PubMedCrossRefGoogle Scholar
  4. 4.
    Ananth, C. V., D. A. Savitz, and M. A. Williams. Placental abruption and its association with hypertension and prolonged rupture of membranes: a methodologic review and meta-analysis. Obstet. Gynecol. 88:309–318, 1996.PubMedCrossRefGoogle Scholar
  5. 5.
    Begonia, M., R. Prabhu, J. Liao, M. Horstemeyer, and L. Williams. The influence of strain rate dependency on the structure–property relations of porcine brain. Ann. Biomed. Eng. 38:3043–3057, 2010.PubMedCrossRefGoogle Scholar
  6. 6.
    Carew, E. O., J. Patel, A. Garg, P. Houghtaling, E. Blackstone, and I. Vesely. Effect of specimen size and aspect ratio on the tensile properties of porcine aortic valve tissues. Ann. Biomed. Eng. 31:526–535, 2003.PubMedCrossRefGoogle Scholar
  7. 7.
    Chames, M. C. M., and M. D. M. Pearlman. Trauma during pregnancy: outcomes and clinical management. Clin. Obstet. Gynecol. 51:398–408, 2008.PubMedCrossRefGoogle Scholar
  8. 8.
    Clemmer, J., J. Liao, D. Davis, M. F. Horstemeyer, and L. N. Williams. A mechanistic study for strain rate sensitivity of rabbit patellar tendon. J. Biomech. 43:2785–2791, 2010.PubMedCrossRefGoogle Scholar
  9. 9.
    Colgan, N. C., M. D. Gilchrist, and K. M. Curran. Applying DTI white matter orientations to finite element head models to examine diffuse TBI under high rotational accelerations. Prog. Biophys. Mol. Biol. 103:304–309, 2010.PubMedCrossRefGoogle Scholar
  10. 10.
    Connolly, A. M., V. L. Katz, K. L. Bash, M. J. McMahon, and W. F. Hansen. Trauma and pregnancy. Am. J. Perinatol. 14:331–336, 1997.PubMedCrossRefGoogle Scholar
  11. 11.
    Daria, C. R. Trauma care and managing the injured pregnant patient. J. Obstet. Gynecol. Neonatal. Nurs. 38:704–714, 2009.CrossRefGoogle Scholar
  12. 12.
    Delotte, J., M. Behr, L. Thollon, P.-J. Arnoux, P. Baque, A. Bongain, and C. Brunet. Pregnant woman and road safety: experimental crash test with post mortem human subject. Surg. Radiol. Anat. 30:185–189, 2008.PubMedCrossRefGoogle Scholar
  13. 13.
    Dighe, M., A. Gokhale, and M. Horstemeyer. Effect of loading condition and stress state on damage evolution of silicon particles in an Al–Si–Mg-base cast alloy. Metall. Mater. Trans. A 33:555–565, 2002.CrossRefGoogle Scholar
  14. 14.
    Duma, S. M. Pregnant Occupants Biomechanics: Advances in Automobile Safety Research. Warrendale, PA: Society of Automotive Engineers, 2010.Google Scholar
  15. 15.
    Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues. New York: Springer, 1981.Google Scholar
  16. 16.
    Gao, Z., and J. P. Desai. Estimating zero-strain states of very soft tissue under gravity loading using digital image correlation. Med. Image Anal. 14:126–137, 2010.PubMedCrossRefGoogle Scholar
  17. 17.
    Hall, D. R. Abruptio placentae and disseminated intravascular coagulopathy. Semin. Perinatol. 33:189–195, 2009.PubMedCrossRefGoogle Scholar
  18. 18.
    Hitosugi, M., Y. Motozawa, M. Kido, T. Yokoyama, H. Kawato, K. Kuroda, and S. Tokudome. Traffic injuries of the pregnant women and fetal or neonatal outcomes. Forensic Sci. Int. 159:51–54, 2006.PubMedCrossRefGoogle Scholar
  19. 19.
    Horstemeyer, M. F., J. Lathrop, A. M. Gokhale, and M. Dighe. Modeling stress state dependent damage evolution in a cast Al–Si–Mg aluminum alloy. Theor. Appl. Fract. Mech. 33:31–47, 2000.CrossRefGoogle Scholar
  20. 20.
    Hu, J., K. D. Klinich, C. S. Miller, G. Nazmi, M. D. Pearlman, L. W. Schneider, and J. D. Rupp. Quantifying dynamic mechanical properties of human placenta tissue using optimization techniques with specimen-specific finite-element models. J. Biomech. 42:2528–2534, 2009.PubMedCrossRefGoogle Scholar
  21. 21.
    Hu, J., K. Klinich, C. Miller, J. Rupp, G. Nazmi, M. Pearlman, and L. Schneider. A stochastic visco-hyperelastic model of human placenta tissue for finite element crash simulations. Ann. Biomed. Eng. 39:1074–1083, 2011.PubMedCrossRefGoogle Scholar
  22. 22.
    Kastelic, J., and E. Baer. Deformation of tendon collagen. In: The Mechanical Properties of Biological Materials, edited by J. F. Vincient, and J. D. Currey. Cambridge: Society for Experimental Biology, 1980, pp. 397–433.Google Scholar
  23. 23.
    Klinich, K. D., C. A. C. Flannagan, J. D. Rupp, M. Sochor, L. W. Schneider, and M. D. Pearlman. Fetal outcome in motor-vehicle crashes: effects of crash characteristics and maternal restraint. Am. J. Obstet. Gynecol. 198:450.e451–450.e459, 2008.CrossRefGoogle Scholar
  24. 24.
    Lee, J. B., and K. H. Yang. Development of a finite element model of the human abdomen. Stapp Car Crash J. 45:79–100, 2001.PubMedGoogle Scholar
  25. 25.
    Liao, J., L. Yang, J. Grashow, and M. S. Sacks. The relation between collagen fibril kinematics and mechanical properties in the mitral valve anterior leaflet. J. Biomech. Eng. 129:78–87, 2007.PubMedCrossRefGoogle Scholar
  26. 26.
    Manoogian, S. J., J. A. Bisplinghoff, C. McNally, A. R. Kemper, A. C. Santago, and S. M. Duma. Dynamic tensile properties of human placenta. J. Biomech. 41:3436–3440, 2008.PubMedCrossRefGoogle Scholar
  27. 27.
    Manoogian, S. J., J. A. Bisplinghoff, C. McNally, A. R. Kemper, A. C. Santago, and S. M. Duma. Effect of strain rate on the tensile material properties of human placenta. J. Biomech. Eng. 131:091008, 2009.PubMedCrossRefGoogle Scholar
  28. 28.
    Mattox, K. L. M. D., and L. M. D. Goetzl. Trauma in pregnancy. Crit. Care Med. Crit. Illn. Pregnancy 33:S385–S389, 2005.Google Scholar
  29. 29.
    Moorcroft, D. M., J. D. Stitzel, G. G. Duma, and S. M. Duma. Computational model of the pregnant occupant: predicting the risk of injury in automobile crashes. Am. J. Obstet. Gynecol. 189:540–544, 2003.PubMedCrossRefGoogle Scholar
  30. 30.
    Moorcroft, D., J. Stitzel, S. Duma, and G. Duma. The effects of uterine ligaments on fetal injury risk in frontal automobile crashes. Proc. Inst. Mech. Eng. D: J. Automob. Eng. 217:1049–1055, 2003.CrossRefGoogle Scholar
  31. 31.
    Motozawa, Y., M. Hitosugi, T. Abe, and S. Tokudome. Effects of seat belts worn by pregnant drivers during low-impact collisions. Am. J. Obstet. Gynecol. 203(1):62.e1–62.e8, 2010.CrossRefGoogle Scholar
  32. 32.
    Nyein, M. K., A. M. Jason, L. Yu, C. M. Pita, J. D. Joannopoulos, D. F. Moore, and R. A. Radovitzky. In silico investigation of intracranial blast mitigation with relevance to military traumatic brain injury. Proc. Natl. Acad. Sci. 107:20703–20708, 2010.PubMedCrossRefGoogle Scholar
  33. 33.
    Oxford, C. M. M., and J. B. Ludmir. Trauma in pregnancy. Clin. Obstet. Gynecol. 52:611–629, 2009.PubMedCrossRefGoogle Scholar
  34. 34.
    Rupp, J. D. K. K., S. Moss, J. Zhou, M. D. Pearlman, and L. W. Schneider. Development and testing of a prototype pregnant abdomen for the small-female hybrid III ATD. Stapp Car Crash J. 45:18, 2001.Google Scholar
  35. 35.
    Viidik, A. Simultaneous mechanical and light microscopic studies of collagen fibers. Zeitschrift fur Anatomie und Entwicklungsgeschichte 136:204–212, 1972.PubMedCrossRefGoogle Scholar
  36. 36.
    Weaver, A. A., K. L. Loftis, S. M. Duma, and J. D. Stitzel. Biomechanical modeling of eye trauma for different orbit anthropometries. J. Biomech. 44:1296–1303, 2011.PubMedCrossRefGoogle Scholar
  37. 37.
    Wren, T. A., and D. R. Carter. A microstructural model for the tensile constitutive and failure behavior of soft skeletal connective tissues. J. Biomech. Eng. 120:55–61, 1998.PubMedCrossRefGoogle Scholar
  38. 38.
    Yamada, H. Strength of Biological Materials. Baltimore: Williams and Wilkinson, 1970.Google Scholar
  39. 39.
    Yu, M., S. Manoogian, S. M. Duma, and J. D. Stitzel. Finite element modeling of human placental tissue. Ann. Adv. Automot. Med. 53:257–270, 2009.PubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2012

Authors and Affiliations

  • Benjamin C. Weed
    • 1
    • 2
  • Ali Borazjani
    • 1
  • Sourav S. Patnaik
    • 1
    • 2
  • R. Prabhu
    • 1
    • 2
  • M. F. Horstemeyer
    • 2
  • Peter L. Ryan
    • 3
  • Thomas Franz
    • 4
  • Lakiesha N. Williams
    • 1
    • 2
  • Jun Liao
    • 1
    • 2
  1. 1.Tissue Bioengineering Laboratory, Department of Agricultural and Biological EngineeringMississippi State UniversityMississippi StateUSA
  2. 2.Center for Advance Vehicular SystemsMississippi State UniversityMississippi StateUSA
  3. 3.Department of Animal and Dairy SciencesMississippi State UniversityMississippi StateUSA
  4. 4.Cardiovascular Research Unit and Centre for Research in Computational and Applied MechanicsUniversity of Cape TownCape TownSouth Africa

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