Free accessMeeting reportFirst published online 2011-5
Biomechanics of the Sensor-Tissue Interface—Effects of Motion,Pressure,and Design on Sensor Performance and Foreign Body Response—Part II: Examples and Application
This article is the second part of a two-part review in which we explore the biomechanics of the sensor-tissue interface as an important aspect of continuous glucose sensor biocompatibility. Part I, featured in this issue of Journal of Diabetes Science and Technology, describes a theoretical framework of how biomechanical factors such as motion and pressure (typically micromotion and micropressure) affect tissue physiology around a sensor and in turn, impact sensor performance. Here in Part II, a literature review is presented that summarizes examples of motion or pressure affecting sensor performance. Data are presented that show how both acute and chronic forces can impact continuous glucose monitor signals. Also presented are potential strategies for countering the ill effects of motion and pressure on glucose sensors. Improved engineering and optimized chemical biocompatibility have advanced sensor design and function, but we believe that mechanical biocompatibility, a rarely considered factor, must also be optimized in order to achieve an accurate, long-term, implantable sensor.
HeltonKLRatnerBDWisniewskiN. Biomechanics of the sensor- tissue interface—effects of motion, pressure and design on sensor performance and the foreign body response—part I: Theoretical framework. J Diabetes Sci Technol.2011;5 (3): 632–46.
2.
MjöbergB. The theory of early loosening of hip prostheses [review]. Orthopedics.1997;20 (12): 1169–75.
3.
WeinbaumSCowinSCZengY. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech.1994;27 (3): 339–60.
4.
Szmukler-MonclerSSalamaHReingewirtzYDubruilleJH. Timing of loading and effect of micromotion on bone-dental implant interface: Review of experimental literature. J Biomed Mater Res.1998;43 (2): 192–203.
5.
HuiskesRWeinansHVanrietbergenB. The relationship between stress shielding and bone resorption around total hip stems and the effects of flexible materials. Clin Orthop Rel Res.1992;274: 124–34.
6.
SøballeKHansenESRasmussenHBJørgensenPHBüngerC. Tissue ingrowth into titanium and hydroxyapatite-coated implants during stable and unstable mechanical conditions. J Orthop Res.1992;10 (2): 285–99.
7.
AspenbergPGoodmanSToksviglarsenSRydLAlbrektssonT. Intermittent micromotion inhibits bone ingrowth. Titanium implants in rabbits. Acta Orthop Scand.1992;63 (2): 141–5.
8.
PrendergastPJHuiskesRSøballeK. Biophysical stimuli on cells during tissue differentiation at implant interfaces. J Biomech.1997;30 (6): 539–48.
9.
GilliganBJShultsMCRhodesRKUpdikeSJ. Evaluation of a subcutaneous glucose sensor out to 3 months in a dog model. Diabetes Care.1994;17 (8): 882–7.
10.
CastleJRWardWK. Amperometric glucose sensors: Sources of error and potential benefit of redundancy. J Diabetes Sci Technol.2010;4 (1): 221–5.
11.
MaurasNBeckRWRuedyKJKollmanCTamborlaneWVChasePBuckinghamBATsalikianEWeinzimerSABoothADXingDY. Lack of accuracy of continuous glucose sensors in healthy, nondiabetic children: Results of the Diabetes Research in Children Network (DirecNet) accuracy study. J Pediatr.2004;144 (6): 770–5.
12.
El-KhatibFHJiangJDamianoER. Automated blood-glucose regulation in diabetic swine using bi-hormonal and insulin-only closed-loop control systems. 69th Scientific Sessions of the American Diabetes Association; 2009 Jun 5–9; New Orleans (LA); 2009. Abstract Number: 426-P.
13.
BretonMDPatekSDFarretAPlaceJDemartiniSBrownSAndersonSKovatchevBPRenardE. Safety supervision system: First clinical trials. Proceedings of the Fourth Advanced Technologies and Treatments for Diabetes Annual Meeting; 2011 Feb 16–19; London, UK. Diabetes Technol Ther.2011;13 (2): 176.
14.
RenardEMFarretAPlaceJCobelliCKovatchevBPBretonMD. Closed-loop insulin delivery using subcutaneous infusion and glucose sensing, and equipped with a dedicated safety supervision algorithm, improves safety of glucose control in type 1 diabetes. Proceedings of the 46th Annual Meeting of the European Association for the Study of Diabetes; 2010 Sep 20–24; Stockholm, Sweden.
15.
PetrofskyJSMcLellanKProwseMBainsGBerkLLeeS. The effect of body fat, aging, and diabetes on vertical and shear pressure in and under a waist belt and its effect on skin blood flow. Diabetes Technol Ther.2010;12 (2): 153–60.
16.
GilliganBCShultsMRhodesRKJacobsPGBraukerJHPintarTJUpdikeSJ. Feasibility of continuous long-term glucose monitoring from a subcutaneous glucose sensor in humans. Diabetes Technol Ther.2004;6 (3): 378–86.
17.
GillettiAMuthuswamyJ. Brain micromotion around implants in the rodent somatosensory cortex. J Neural Eng.2006;3 (3): 189–95.
18.
GargSKSchwartzSEdelmanSV. Improved glucose excursions using an implantable real-time continuous glucose sensor in adults with type 1 diabetes. Diabetes Care.2004;27 (3): 734–8.
19.
KvistPHIburgTDawsonHDJensenHE. Effect of subcutaneous glucose sensor implantation on skin mRNA expression in pigs. Diabetes Technol Ther.2010;12 (10): 791–9.
20.
WardWKTroupeJE. Assessment of chronically implanted subcutaneous glucose sensors in dogs: The effect of surrounding fluid masses. ASAIO J.1999;45 (6): 555–61.
21.
KoschwanezHEYapFYKlitzmanBReichertWM. In vitro and in vivo characterization of porous poly-L-lactic acid coatings for subcutaneously implanted glucose sensors. J Biomed Mater Res A.2008;87 (3): 792–807.
22.
KoschwanezHEReichertWMKlitzmanB. Intravital microscopy evaluation of angiogenesis and its effects on glucose sensor performance. J Biomed Mater Res A.2010;93 (4): 1348–57.
JuYMYuBZWestLMoussyYMoussyF. A novel porous collagen scaffold around an implantable biosensor for improving biocompatibility. II. Long-term in vitro/in vivo sensitivity characteristics of sensors with NDGA- or GA-crosslinked collagen scaffolds. J Biomed Mater Res A.2010;92 (2): 650–8.
25.
HenningT. Commercially available continuous glucose monitoring systems. In: CunninghamDDStenkenJA, editors. In vivo glucose sensing, volume 174. Hoboken (NJ): John Wiley & Sons, Inc.; 2009.
26.
PrichardHLSchroederTReichertWMKlitzmanB. Bioluminescence imaging of glucose in tissue surrounding polyurethane and glucose sensor implants. J Diabetes Sci Technol.2010;4 (5): 1055–62.
27.
KluehULiuZHChoBOuyangTMFeldmanBHenningTPKaurMKreutzerD. Continuous glucose monitoring in normal mice and mice with prediabetes and diabetes. Diabetes Technol Ther.2006;8 (3): 402–12.
28.
AndersonJM. Biological responses to materials [review]. Ann Rev Mater Res.2001;31: 81–110.
29.
Thomé-DuretVAussedatBReachGGangnerauMNLemonnierFKleinJCZhangYHuYWilsonGS. Continuous glucose monitoring in the free-moving rat. Metabolism.1998;47 (7): 799–803.
30.
WardWKJansenLBAndersonEReachGKleinJCWilsonGS. A new amperometric glucose microsensor: in vitro and short-term in vivo evaluation. Biosens Bioelectron.2002;17 (3): 181–9.
31.
SubbaroyanJMartinDCKipkeDR. A finite-element model of the mechanical effects of implantable microelectrodes in the cerebral cortex. J Neural Eng.2005;2 (4): 103–13.
32.
KvistPHIburgTBieleckiMGerstenbergMBuch-RasmussenTHasselagerEJensenHE. Biocompatibility of electrochemical glucose sensors implanted in the subcutis of pigs. Diabetes Technol Ther.2006;8 (4): 463–75.
33.
UpdikeSJShultsMCGilliganBJRhodesRK. A subcutaneous glucose sensor with improved longevity, dynamic range, and stability of calibration. Diabetes Care.2000;23 (2): 208–14.
34.
MaynardEMFernandezENormannRA. A technique to prevent dural adhesions to chronically implanted microelectrode arrays. J Neurosci Methods.2000;97 (2): 93–101.
35.
MahmudJHoltCAEvansSL. An innovative application of a small-scale motion analysis technique to quantify human skin deformation in vivo. J Biomech.2010;43 (5): 1002–6.
36.
Von RecumA. New aspects of biocompatibility: Motion at the interface. In: LeeAJCHeimkeBSolteszU, editors. Clinical implant materials: Proceedings of the Eighth European Conference on Biomaterials, 1989 Sep 7–9; Heidelberg, Germany. Amsterdam; New York: Elsevier Science Pub. Co; 1990.
37.
GantRMAbrahamAAHouYCumminsBMGrunlanMACotéGL. Design of a self-cleaning thermoresponsive nanocomposite hydrogel membrane for implantable biosensors. Acta Biomater.2010;6 (8): 2903–10.
38.
YuBZLongNMoussyYMoussyF. A long-term flexible minimally-invasive implantable glucose biosensor based on an epoxy-enhanced polyurethane membrane. Biosens Bioelectron.2006;21 (12): 2275–82.
39.
HilbornJBjurstenLM. A new and evolving paradigm for biocompatibitity. J Tissue Eng Regen Med.2007;1 (2): 110–9.
40.
SandersJEBaleSDNeumannT. Tissue response to microfibers of different polymers: Polyester, polyethylene, polylactic acid, and polyurethane. J Biomed Mater Res.2002;62 (2): 222–7.
41.
GeerligsMPetersGWAckermansPAOomensCWBaaijensFP. Does subcutaneous adipose tissue behave as an (anti-)thixotropic material?J Biomech.2010;43 (6): 1153–9.
42.
AgachePGMonneurCLevequeJLDerigalJ. Mechanical properties and Young's modulus of human skin in vivo. Arch Dermatol Res.1980;269 (3): 221–32.
43.
BarelACourageWClarysP. Suction method for measurment of skin mechanical: The cutometer. In: SerupJJemecG, editors. Handbook of non-invasive methods and the skin. Boca Raton (FL): CRC Press; 1995. p. 335–40.
44.
DiridollouSBersonMVabreVBlackDKarlssonBAuriolFGregoireJMYvonCVaillantLGallYPatatF. An in vivo method for measuring the mechanical properties of the skin using ultrasound. Ultrasound Med Biol.1998;24 (2): 215–24.
45.
DiridollouSBlackDLagardeJMGallYBersonMVabreVPatatFVaillantL. Sex- and site-dependent variations in the thickness and mechanical properties of human skin in vivo. Int J Cosmet Sci.2000;22 (6): 421–35.
46.
GennissonJLBaldeweckTTanterMCathelineSFinkMSandrinLCornillonCQuerleuxB. Assessment of elastic parameters of human skin using dynamic elastography. IEEE Trans Ultrason Ferroelectr Freq Control.2004;51 (8): 980–9.
47.
HendriksFMBrokkenDvan EemerenJOomensCWJBaaijensFPTHorstenJ. A numerical-experimental method to characterize the non-linear mechanical behaviour of human skin. Skin Res Technol.2003;9 (3): 274–83.
48.
PatelPNSmithCKPatrickCW. Rheological and recovery properties of poly(ethylene glycol) diacrylate hydrogels and human adipose tissue. J Biomed Mater Res A.2005;73 (3): 313–9.
49.
Van HoutenEEWDoyleyMMKennedyFEWeaverJBPaulsenKD. Initial in vivo experience with steady-state subzone-based MR elastography of the human breast. J Magn Reson Imaging.2003;17 (1): 72–85.
50.
WuJZCutlipRGWelcomeDDongRG. Estimation of the viscous properties of skin and subcutaneous tissue in uniaxial stress relaxation tests. Biomedical Mater Eng.2006;16 (1): 53–66.
51.
WuKSvan OsdolWWDauskardtRH. Mechanical properties of human stratum corneum: Effects of temperature, hydration, and chemical treatment. Biomaterials.2006;27 (5): 785–95.
52.
LevensonSMGeeverEFCrowleyLVOatesJF3rdBerardCWRosenH. The healing of rat skin wounds. Ann Surg.1965;161: 293–308.
53.
BraukerJHCarr-BrendelVEMartinsonLACrudeleJJohnstonWDJohnsonRC. Neovascularization of synthetic membranes directed by membrane microarchitecture. J Biomed Mater Res.1995;29 (12): 1517–24.
54.
MarshallAJIrvinCABarkerTSageEHHauchKDRatnerBD. Biomaterials with tightly controlled pore size that promote vascular in-growth. Polym Prepr.2004;45 (2): 100–1.
55.
PichaGJDrakeRF. Pillared-surface microstructure and soft-tissue implants: Effect of implant site and fixation. J Biomed Mater Res.1996;30 (3): 305–12.
56.
SharkawyAAKlitzmanBTruskeyGAReichertWM. Engineering the tissue which encapsulates subcutaneous implants. II. Plasma-tissue exchange properties. J Biomed Mater Res.1998;40 (4): 586–97.
57.
UpdikeSJShultsMCGilliganBJRhodesRK. A subcutaneous glucose sensor with improved longevity, dynamic range, and stability of calibration. Diabetes Care.2000;23 (2): 208–14.
58.
WardWKSlobodzianEPTiekotterKLWoodMD. The effect of microgeometry, implant thickness and polyurethane chemistry on the foreign body response to subcutaneous implants. Biomaterials.2002;23 (21): 4185–92.
59.
SandersJEStilesCEHayesCL. Tissue response to single-polymer fibers of varying diameters: Evaluation of fibrous encapsulation and macrophage density. J Biomed Mater Res.2000;52 (1): 231–7.
60.
VaddirajuSTomazosIBurgessDJJainFCPapadimitrakopoulosF. Emerging synergy between nanotechnology and implantable biosensors: A review. Biosens Bioelectron.2010;25 (7): 1553–65.
61.
SandersJERochefortJR. Fibrous encapsulation of single polymer microfibers depends on their vertical dimension in subcutaneous tissue. J Biomed Mater Res A.2003;67 (4): 1181–7.
62.
HoltBTripathiAMorganJ. Viscoelastic response of human skin to low magnitude physiologically relevant shear. J Biomech.2008;41 (12): 2689–95.
63.
MatlagaBFYasenchakLPSalthouseTN. Tissue response to implanted polymers: The significance of sample shape. J Biomed Mater Res.1976;10 (3): 391–7.
64.
NovakMTYuanFReichertWM. Modeling the relative impact of capsular tissue effects on implanted glucose sensor time lag and signal attenuation. Anal Bioanal Chem.2010;398 (4): 1695–705.
