What Is Considered a Variation of Biomechanical Parameters in Tensile Tests of Collagen-Rich Human Soft Tissues?—Critical Considerations Using the Human Cranial Dura Mater as a Representative Morpho-Mechanic Model

Abstract

Background and Objectives: Profound knowledge on the load-dependent behavior of human soft tissues is required for the development of suitable replacements as well as for realistic computer simulations. Regarding the former, e.g., the anisotropy of a particular biological tissue has to be represented with site- and direction-dependent particular mechanical values. Contrary to this concept of consistent mechanical properties of a defined soft tissue, mechanical parameters of soft tissues scatter considerably when being determined in tensile tests. In spite of numerous measures taken to standardize the mechanical testing of soft tissues, several setup- and tissue-related factors remain to influence the mechanical parameters of human soft tissues to a yet unknown extent. It is to date unclear if measurement extremes should be considered a variation or whether these data have to be deemed incorrect measurement outliers. This given study aimed to determine mechanical parameters of the human cranial dura mater as a model for human soft tissues using a highly standardized protocol and based on this, critically evaluate the definition for the term mechanical “variation” of human soft tissue. Materials and Methods: A total of 124 human dura mater samples with an age range of 3 weeks to 94 years were uniformly retrieved, osmotically adapted and mechanically tested using customized 3D-printed equipment in a quasi-static tensile testing setup. Scanning electron microscopy of 14 samples was conducted to relate the mechanical parameters to morphological features of the dura mater. Results: The here obtained mechanical parameters were scattered (elastic modulus = 46.06 MPa, interquartile range = 33.78 MPa; ultimate tensile strength = 5.56 MPa, interquartile range = 4.09 MPa; strain at maximum force = 16.58%, interquartile range = 4.81%). Scanning electron microscopy revealed a multi-layered nature of the dura mater with varying fiber directions between its outer and inner surface. Conclusions: It is concluded that mechanical parameters of soft tissues such as human dura mater are highly variable even if a highly standardized testing setup is involved. The tissue structure and composition appeared to be the main contributor to the scatter of the mechanical parameters. In consequence, mechanical variation of soft tissues can be defined as the extremes of a biomechanical parameter due to an uncontrollable change in tissue structure and/or the respective testing setup.

Systematic review and meta-analysis of the biomechanical properties of the human dura mater applicable in computational human head models

“…These were published between 1970 and 2020. Of these, 13 studies were conducted on cranial (Aydin et al 2019 ; Galford and McElhaney 1970 ; Kizmazoglu et al 2019 ; McGarvey et al 1984 ; Melvin et al 1970 ; Sacks et al 1998 ; van Noort et al 1981 ; Wolfinbarger et al 1994 ; Yamada et al 1997 ; Zwirner et al 2019a , b , c , 2020 ) and 4 on spinal dura mater (Patin et al 1993 ; Runza et al 1999 ; Tencer et al 1985 ; Zarzur 1996 ), respectively. A summary of the retrieved information from the searched studies is given in Table 1 .…”

“…The sample characteristics varied between studies. The number of mechanically investigated samples ranged from 7 (Aydin et al 2019 ) to 124 (Zwirner et al 2020 ). Cadaver numbers ranged from 5 (Sacks et al 1998 ) to 75 (Zwirner et al 2020 ).…”

“…The number of mechanically investigated samples ranged from 7 (Aydin et al 2019 ) to 124 (Zwirner et al 2020 ). Cadaver numbers ranged from 5 (Sacks et al 1998 ) to 75 (Zwirner et al 2020 ). In one case, the difference between tested samples and number of investigated cadavers was not stated clearly (Melvin et al 1970 ).…”

“…Several factors give rise to the lack of information available, including but not limited to the availability of fresh cadaveric tissues, the expertise of research teams in anatomy and engineering or financial challenges to buy required testing equipment. As a prime example, the biomechanical characterization of the dura mater was investigated further throughout the past three years (Aydin et al 2019 ; Kizmazoglu et al 2019 ; Zwirner et al 2019a , b , c , 2020 ). The biomechanical properties of cranial dura mater are paramount to select and fabricate appropriate artificial substitutes for duraplasty, such as the Gore-Tex Expanded Cardiovascular Patch (W.L.…”

“…Gore & Associates Inc., Flagstaff, AZ, USA), the Durepair graft (Medtronic Inc., Goleta, CA, USA), or the Tutopatch (Tutogen Medical GmbH, Neunkirchen am Brand, Germany) (Kizmazoglu et al 2019 ). Furthermore, the biomechanical properties of the dura mater are required when it is used as a “model tissue” to answer fundamental research questions on the material behavior of collagen-rich tissues (Zwirner et al 2019a , 2020 ). Moreover, the biomechanical properties of cranial dura mater are required to accurately simulate the tissue in computational head models to answer predominantly impact-related research questions (Chafi et al 2009 ; Kizmazoglu et al 2019 ; Viano et al 2005 ; Zhang et al 2001a ).…”