Abstract
This study investigated the impact of type 2 diabetes and diabetic peripheral neuropathy on grip force control during object manipulation. The study included three age-matched groups: type 2 diabetes alone (n = 11), type 2 diabetes with neuropathy (n = 13), and healthy controls (n = 12). Grip force control variables derived from lifting and holding an experimental cup were the ratio between grip force and load forces during lifting (GFR), latency 1 and latency 2, which represented the time between the object’s grip and its lift-off from the table, and the period between object’s lift-off and the grip force peak, respectively; time lag, which denoted the time difference between the grip and load force peaks during the lifting phase, and finally static force, which was the grip force average during the holding phase. Grip force control variables were compared between groups using one-way ANOVA and Kruskal–Wallis test. Post-hoc analysis was used to compare differences between groups. GFR and latency 1 showed significant differences between groups; the type 2 diabetes with neuropathy group showed larger GFR than the type 2 diabetes alone and healthy control groups. The latency 1was longer for the group with neuropathy in comparison with the health control group. There were no significant differences between groups for latency 2, time lag, and static force. Our results showed impaired GFR and latency 1 in participants with type 2 diabetes with neuropathy while the time lag was preserved. People with type 2 diabetes alone might not have any deficits in grip force control. Higher grip forces might expose people with type 2 diabetes and diabetic peripheral neuropathy to the risk of fatigue and injuring their hands. Future studies should investigate strategies to help people with type 2 diabetes with neuropathy adjust grip forces during object manipulation.
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References
Alberts JL, Elder CM, Okun MS, Vitek JL (2004) Comparison of pallidal and subthalamic stimulation on force control in patient’s with Parkinson’s disease. Mot Control 8:484–499
Association AD (2018) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2018. Diabetes Care 41:S13–S27. https://doi.org/10.2337/dc18-S002
Augurelle A-S, Smith AM, Lejeune T, Thonnard J-L (2003) Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. J Neurophysiol 89:665–671
Bales JG, Meals R (2009) Peripheral neuropathy of the upper extremity: medical comorbidity that confounds common orthopedic pathology. Orthopedics. https://doi.org/10.3928/01477447-20090818-19
Baugh LA, Yak A, Johansson RS, Flanagan JR (2016) Representing multiple object weights: competing priors and sensorimotor memories. J Neurophysiol 116:1615–1625. https://doi.org/10.1152/jn.00282.2016
Bays HE, Chapman RH, Grandy S, Group SI (2007) The relationship of body mass index to diabetes mellitus, hypertension and dyslipidaemia: comparison of data from two national surveys. Int J Clin Pract 61:737–747. https://doi.org/10.1111/j.1742-1241.2007.01336.x
Berner J, Schonfeldt-Lecuona C, Nowak DA (2007) Sensorimotor memory for fingertip forces during object lifting: the role of the primary motor cortex. Neuropsychologia 45:1931–1938. https://doi.org/10.1016/j.neuropsychologia.2006.11.011
Blennerhassett JM, Carey LM, Matyas TA (2008) Clinical measures of handgrip limitation relate to impaired pinch grip force control after stroke. J Hand Ther. https://doi.org/10.1197/j.jht.2007.10.021
Cederlund RI, Thomsen N, Thrainsdottir S, Eriksson K-F, Sundkvist G, Dahlin LB (2009) Hand disorders, hand function, and activities of daily living in elderly men with type 2 diabetes. J Diabetes Complications 23:32–39. https://doi.org/10.1016/j.jdiacomp.2007.09.002
Chen B, Lee YJ, Aruin AS (2016) Control of grip force and vertical posture while holding an object and being perturbed. Exp Brain Res 234:3193–3201. https://doi.org/10.1007/s00221-016-4717-2
Chiu HY, Hsu HY, Kuo LC, Su FC, Yu HI, Hua SC, Lu CH (2014) How the impact of median neuropathy on sensorimotor control capability of hands for diabetes: an achievable assessment from functional perspectives. PLoS ONE 9:e94452. https://doi.org/10.1371/journal.pone.0094452
Claudino R, Mazo GZ, Santos MJ (2013) Age-related changes of grip force control in physically active adults. Percept Mot Skills 116:859–871. https://doi.org/10.2466/10.06.pms.116.3.859-871
Cole KJ, Rotella DL, Harper JG (1999) Mechanisms for age-related changes of fingertip forces during precision gripping and lifting in adults. J Neurosci 19:3238–3247
Connell LA, Tyson S (2012) Measures of sensation in neurological conditions: a systematic review. Clin Rehabil 26:68–80
de Freitas PB, Lima KC (2013) Grip force control during simple manipulation tasks in non-neuropathic diabetic individuals. Clin Neurophysiol 124:1904–1910. https://doi.org/10.1016/j.clinph.2013.04.002
de Almeida Lima KC, da Silva BL, Hatanaka E, Rolim LC, de Freitas PB (2017) Grip force control and hand dexterity are impaired in individuals with diabetic peripheral neuropathy. Neurosci Lett 659:54–59
de Oliveira DG, Nunes PM, Aruin AS, Dos Santos MJ (2011) Grip force control in individuals with hand osteoarthritis. J Hand Ther. https://doi.org/10.1016/j.jht.2011.06.002
Dyck PJ, Albers JW, Andersen H et al (2011) Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev 27:620–628. https://doi.org/10.1002/dmrr.1226
Fellows SJ, Noth J, Schwarz M (1998) Precision grip and Parkinson’s disease. Brain 121(Pt 9):1771–1784. https://doi.org/10.1093/brain/121.9.1771
Fellows SJ, Ernst J, Schwarz M, Topper R, Noth J (2001) Precision grip deficits in cerebellar disorders in man. Clin Neurophysiol 112:1793–1802
Feng Y, Schlosser FJ, Sumpio BE (2009) The Semmes Weinstein monofilament examination as a screening tool for diabetic peripheral neuropathy. J Vasc Surg. https://doi.org/10.1016/j.jvs.2009.05.017
Flanagan JR, Tresilian JR (1994) Grip-load force coupling: a general control strategy for transporting objects. J Exp Psychol Hum Percept Perform 20:944–957
Flanagan JR, Wing AM (1993) Modulation of grip force with load force during point-to-point arm movements. Exp Brain Res 95:131–143. https://doi.org/10.1007/BF00229662
Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17:1519–1528
Flanagan JR, King S, Wolpert DM, Johansson RS (2001) Sensorimotor prediction and memory in object manipulation. Can J Exp Psychol 55:87–95. https://doi.org/10.1037/h0087355
Frenkel-Toledo S, Yamanaka J, Friedman J, Feldman AG, Levin MF (2019) Referent control of anticipatory grip force during reaching in stroke: an experimental and modeling study. Exp Brain Res 237:1655–1672. https://doi.org/10.1007/s00221-019-05498-y
Hager-Ross C, Johansson RS (1996) Nondigital afferent input in reactive control of fingertip forces during precision grip. Exp Brain Res 110:131–141. https://doi.org/10.1007/BF00241382
Hazari MAH, Ram Reddy B, Uzma N, Santhosh Kumar B (2015) Cognitive impairment in type 2 diabetes mellitus. Int J Diabetes Mellitus 3:19–24. https://doi.org/10.1016/j.ijdm.2011.01.001
Hermsdörfer J, Hagl E, Nowak D, Marquardt C (2003) Grip force control during object manipulation in cerebral stroke. Clin Neurophysiol 114:915–929
Hermsdorfer J, Hagl E, Nowak DA (2004) Deficits of anticipatory grip force control after damage to peripheral and central sensorimotor systems. Hum Mov Sci 23:643–662. https://doi.org/10.1016/j.humov.2004.10.005
Hsu HY, Chiu HY, Lin HT, Su FC, Lu CH, Kuo LC (2015) Impacts of elevated glycaemic haemoglobin and disease duration on the sensorimotor control of hands in diabetes patients. Diabetes Metab Res Rev 31:385–394. https://doi.org/10.1002/dmrr.2623
Iyengar V, Santos MJ, Ko M, Aruin AS (2009) Grip force control in individuals with multiple sclerosis. Neurorehabil Neural Repair 23:855–861. https://doi.org/10.1177/1545968309338194
Johansson RS (2002) Dynamic use of tactile afferent signals in control of dexterous manipulation. Adv Exp Med Biol 508:397–410. https://doi.org/10.1007/978-1-4615-0713-0_45
Johansson RS, Flanagan JR (2009) Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10:345–359. https://doi.org/10.1038/nrn2621
Johansson RS, Vallbo A (1979) Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283–300
Johnson KO, Phillips JR (1981) Tactile spatial resolution. I. Two-point discrimination, gap detection, grating resolution, and letter recognition. J Neurophysiol 46:1177–1192. https://doi.org/10.1152/jn.1981.46.6.1177
Lemke C, Matthaei S (2009) The point-of-care (POC) A1CNow+ device: precision and accuracy of an improved version. In: Diabetes, volume 58. AMER DIABETES ASSOC 1701 N BEAUREGARD ST, ALEXANDRIA, VA 22311–1717 USA, pp A111-A111
Lima KCA, Santos GOC, Donato SSV, Borges L, Hatanaka E, de Freitas PB (2021) Grip and load force control and coordination in individuals with diabetes in different manipulation tasks. Hum Mov Sci 77:102793. https://doi.org/10.1016/j.humov.2021.102793
Lowe BD, Freivalds A (1999) Effect of carpal tunnel syndrome on grip force coordination on hand tools. Ergonomics 42:550–564. https://doi.org/10.1080/001401399185469
Marneweck M, Barany DA, Santello M, Grafton ST (2018) Neural representations of sensorimotor memory- and digit position-based load force adjustments before the onset of dexterous object manipulation. J Neurosci 38:4724–4737. https://doi.org/10.1523/JNEUROSCI.2588-17.2018
Matsutomo R, Takebayashi K, Aso Y (2005) Assessment of peripheral neuropathy using measurement of the current perception threshold with the neurometer in patients with type 2 diabetes mellitus. J Int Med Res 33:442–453
Mattos DJ, Domenech SC, Borges Junior NG, Santos MJ (2012) Effect of fatigue on grip force control during object manipulation in carpal tunnel syndrome. Mot Control 16:521–536. https://doi.org/10.1123/mcj.16.4.521
Meijer JW, van Sonderen E, Blaauwwiekel EE, Smit AJ, Groothoff JW, Eisma WH, Links TP (2000) Diabetic neuropathy examination: a hierarchical scoring system to diagnose distal polyneuropathy in diabetes. Diabetes Care 23:750–753
Monzee J, Lamarre Y, Smith AM (2003) The effects of digital anesthesia on force control using a precision grip. J Neurophysiol 89:672–683. https://doi.org/10.1152/jn.00434.2001
Novak CB (2001) Evaluation of hand sensibility: a review. J Hand Ther 14:266–272
Nowak DA, Hermsdorfer J (2003) Selective deficits of grip force control during object manipulation in patients with reduced sensibility of the grasping digits. Neurosci Res 47:65–72
Nowak DA, Hermsdorfer J (2005) Grip force behavior during object manipulation in neurological disorders: toward an objective evaluation of manual performance deficits. Mov Disord 20:11–25. https://doi.org/10.1002/mds.20299
Nowak DA, Hermsdorfer J (2006) Objective evaluation of manual performance deficits in neurological movement disorders. Brain Res Rev 51:108–124. https://doi.org/10.1016/j.brainresrev.2005.10.003
Nowak DA, Hermsdorfer J, Glasauer S, Philipp J, Meyer L, Mai N (2001) The effects of digital anaesthesia on predictive grip force adjustments during vertical movements of a grasped object. Eur J Neurosci 14:756–762
Nowak DA, Hermsdorfer J, Marquardt C, Fuchs HH (2002) Grip and load force coupling during discrete vertical arm movements with a grasped object in cerebellar atrophy. Exp Brain Res 145:28–39. https://doi.org/10.1007/s00221-002-1079-8
Nowak DA, Glasauer S, Hermsdorfer J (2004) How predictive is grip force control in the complete absence of somatosensory feedback? Brain 127:182–192
Nowak DA, Glasauer S, Hermsdorfer J (2013) Force control in object manipulation–a model for the study of sensorimotor control strategies. Neurosci Biobehav Rev 37:1578–1586. https://doi.org/10.1016/j.neubiorev.2013.06.003
Nunes PM, de Oliveira DG, Aruin AS, dos Santos MJ (2012) Relationship between hand function and grip force control in women with hand osteoarthritis. J Rehabil Res Dev 49:855–865
Olaleye D, Perkins BA, Bril V (2001) Evaluation of three screening tests and a risk assessment model for diagnosing peripheral neuropathy in the diabetes clinic. Diabetes Res Clin Pract 54:115–128
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Perkins BA, Olaleye D, Zinman B, Bril V (2001) Simple screening tests for peripheral neuropathy in the diabetes clinic. Diabetes Care 24:250–256
Quaney BM, Rotella DL, Peterson C, Cole KJ (2003) Sensorimotor memory for fingertip forces: evidence for a task-independent motor memory. J Neurosci 23:1981–1986
Raghavan P, Krakauer JW, Gordon AM (2006) Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunar syndrome. Brain 129:1415–1425. https://doi.org/10.1093/brain/awl070
Rucker JL, McDowd JM, Kluding PM (2012) Executive function and type 2 diabetes: putting the pieces together. Phys Ther 92:454–462. https://doi.org/10.2522/ptj.20100397
Selvarajah D, Tesfaye S (2006) Central nervous system involvement in diabetes mellitus. Curr Diab Rep 6:431–438
Selvarajah D, Wilkinson ID, Emery CJ et al (2006) Early involvement of the spinal cord in diabetic peripheral neuropathy. Diabetes Care 29:2664–2669. https://doi.org/10.2337/dc06-0650
Selvarajah D, Wilkinson ID, Maxwell M et al (2014) Magnetic resonance neuroimaging study of brain structural differences in diabetic peripheral neuropathy. Diabetes Care 37:1681–1688. https://doi.org/10.2337/dc13-2610
Serrien DJ, Wiesendanger M (2001) Bimanual organization of manipulative forces: evidence from erroneous feedforward programming of precision grip. Eur J Neurosci 13:1825–1832. https://doi.org/10.1046/j.0953-816x.2001.01548.x
Thonnard J-L, Saels P, Van den Bergh P, Lejeune T (1999) Effects of chronic median nerve compression at the wrist on sensation and manual skills. Exp Brain Res 128:61–64
Watkins PJ, Thomas PK (1998) Diabetes mellitus and the nervous system. J Neurol Neurosurg Psychiatry 65:620–632
Wenzelburger R, Kopper F, Frenzel A et al (2005) Hand coordination following capsular stroke. Brain 128:64–74. https://doi.org/10.1093/brain/awh317
Zhang Y, Li J, Wang T, Wang J (2014) Amplitude of sensory nerve action potential in early stage diabetic peripheral neuropathy: an analysis of 500 cases. Neural Regen Res 9:1389–1394. https://doi.org/10.4103/1673-5374.137593
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dos Santos, M., Yahya, A., Kluding, P. et al. The effect of type 2 diabetes and diabetic peripheral neuropathy on predictive grip force control. Exp Brain Res 241, 2605–2616 (2023). https://doi.org/10.1007/s00221-023-06705-7
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DOI: https://doi.org/10.1007/s00221-023-06705-7