Characterizing Nipple Biomechanics: In Search of an Ideal Tissue Substitute

Abstract

INTRODUCTION: Following total mastectomy, nipple reconstruction is an essential, often last step of breast reconstruction. The positive psychological effect is critical to the recovery process, and patients report increased satisfaction, with increased happiness in sexual behavior and their nude appearance. As is the case for most reconstructive surgeries, use of autologous tissue is the ideal reconstructive methodology, eliminating the possibility of rejection, minimizing infection, and maximizing tissue integration and permanence. Autologous costal cartilage (CC) grafts have been used to maintain neo-nipple projection, but this technique is suboptimal due to difficulty of controlling the size and shape of the neo-nipple and stiff biomechanical qualities of resultant neo-nipple. We have previously shown the efficacy of minced CC in preservation of neo-nipple projection when integrated with external biodegradable scaffold. Herein, we assess simple and reliable methodologies for mechanical processing of CC to achieve desired biomechanical characteristics that mimic the human nipple more closely. METHODS: Excess CC, from patients undergoing deep inferior epigastric flap procedure, was mechanically processed by either shredding or mincing in sterile fashion. Mechanically processed cartilage was either packed into a custom-designed, 3D-printed external scaffolds (made from polylactic acid), or an equal volume was wrapped in Surgicel. The constructs were implanted into nude rats by creating a subcutaneous pocket using CV flap technique. The constructs were explanted after 3 months for histologic and biomechanical testing. Biomechanical testing was also performed on native human nipple and premanipulation/implantation CC. Confined compression testing was performed by compressing the samples to 30% of their original height in 6 steps of 5% strain, with 10 minutes between steps to allow for full stress relaxation. Equilibrium modulus was calculated. RESULTS: After 3 months in vivo, mechanical analysis demonstrated that mincing of the cartilage changed the equilibrium modulus and hydraulic permeability of implants to values closer to native human nipple regardless of presence of the external scaffold. The minced CC possessed almost 4 times smaller modulus than the premanipulation/implantation CC on average (702 versus 2,723 kPa; P = 0.0036). The average human nipple had lower, but not statistically significant, equilibrium modulus than the minced cartilage (257 versus 702 kPa). Hematoxylin/eosin staining and LIVE/DEAD assay showed the presence of healthy and viable cartilage in all groups. There was evidence of fibrovascular tissue invasion resulting in consolidation and incorporation of the implants. CONCLUSIONS: We demonstrate that autologous CC, usually discarded during a deep inferior epigastric flap procedure, can be used as a viable implant for nipple reconstruction. Because the original CC is firm and nonmalleable, mechanical processing of the CC reduces stiffness and allows for incorporation of individualized engineered constructs tailored to patient desire (sizes/levels of projection). We demonstrated that the mincing of CC resulted in constructs with more similar biomechanical properties to that of the native human nipple without the loss of projection or topography seen with traditional approaches to nipple reconstruction.