Skip to main content
Top
Published in: Neurological Sciences 7/2021

01-07-2021 | Neuropathic Pain | Original Article

The increase of neuropathic symptoms in diabetic patients is related with osteopenia

Authors: Elif Börekci, Adem Kara, Mahmut Kılıç, Nermin Tanık, Zeynep T. Ozan, Tekin Yıldırım, Yalçın Aral

Published in: Neurological Sciences | Issue 7/2021

Login to get access

Abstract

Purpose

To investigate the relationship between the intensity of neuropathic pain and the severity of osteopenia in type 2 diabetic patients with painful diabetic peripheral neuropathy (painful DPN).

Methods

In 220 patients with type 2 diabetes included in the screening, the presence of neuropathic pain was evaluated using the Douleur Neuropathique 4 Questions (DN4) scoring system. One hundred forty-five patients with painful DPN were identified and included in the study. Socio-demographic and laboratory evaluations were made and bone mineral density (BMD) of these patients was evaluated by the dual-energy x-ray absorptiometry (DEXA) method.

Results

There was a significant correlation between the neuropathic pain score and the total T scores of the lumbar spine and femur in patients with painful DPN. According to the regression analysis (standard coefficients), the DN4 score (0.498); the level of vitamin D (− 0.246) and the female sex (0.236) for the lumbar spine region; age (0.387); DN4 score (0.261); and vitamin D level (− 0.155) for the femur region were independently influencing factors on the development of osteoporosis. When osteoporosis (T score ≤ − 2.5) of the lumbar spine was analyzed by binary logistic regression, the risk of osteoporosis in women was 4.4 times higher, and the risk increased with increasing DN4 score.

Conclusion

The increase of neuropathic symptoms in patients with DPN is an effective and important factor in the development of diabetic osteopenia.
Literature
1.
go back to reference Juster-Switlyk K, Smith AG. (2016) Updates in diabetic peripheral neuropathy. F1000Res. 5:F1000 Faculty Rev-738. Juster-Switlyk K, Smith AG. (2016) Updates in diabetic peripheral neuropathy. F1000Res. 5:F1000 Faculty Rev-738.
2.
go back to reference Van Acker K, Bouhassira D, De Bacquer D, Weiss S, Matthys K, Raemen H et al (2009) Prevalence and impact on quality of life of peripheral neuropathy with or without neuropathic pain in type 1 and type 2 diabetic patients attending hospital outpatients clinics. Diabetes Metab. 35(3):206–213CrossRef Van Acker K, Bouhassira D, De Bacquer D, Weiss S, Matthys K, Raemen H et al (2009) Prevalence and impact on quality of life of peripheral neuropathy with or without neuropathic pain in type 1 and type 2 diabetic patients attending hospital outpatients clinics. Diabetes Metab. 35(3):206–213CrossRef
3.
go back to reference Boulton AJM, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D, American Diabetes Association (2005) Diabetic neuropathies. A statement by the American Diabetes Association. Diabetes Care. 28(4):956–962CrossRef Boulton AJM, Vinik AI, Arezzo JC, Bril V, Feldman EL, Freeman R, Malik RA, Maser RE, Sosenko JM, Ziegler D, American Diabetes Association (2005) Diabetic neuropathies. A statement by the American Diabetes Association. Diabetes Care. 28(4):956–962CrossRef
4.
go back to reference Schreiber AK, Nones CF, Reis RC, Chichorro JG, Cunha JM (2015) Diabetic neuropathic pain: physiopathology and treatment. World J Diabetes. 6(3):432–444CrossRefPubMedCentral Schreiber AK, Nones CF, Reis RC, Chichorro JG, Cunha JM (2015) Diabetic neuropathic pain: physiopathology and treatment. World J Diabetes. 6(3):432–444CrossRefPubMedCentral
5.
go back to reference Edwards JL, Vincent AM, Cheng HT, Feldman EL (2008) Diabetic neuropathy: mechanisms to management. Pharmacol Ther. 120(1):1–34CrossRefPubMedCentral Edwards JL, Vincent AM, Cheng HT, Feldman EL (2008) Diabetic neuropathy: mechanisms to management. Pharmacol Ther. 120(1):1–34CrossRefPubMedCentral
6.
go back to reference Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 18(4):427–444CrossRef Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 18(4):427–444CrossRef
7.
go back to reference Forst T, Pfutzner A, Kann P, Schehler B, Lobmann R, Schafer H et al (1995) Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabetic medicine: a journal of the British Diabetic Association. 12(10):874–879CrossRef Forst T, Pfutzner A, Kann P, Schehler B, Lobmann R, Schafer H et al (1995) Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabetic medicine: a journal of the British Diabetic Association. 12(10):874–879CrossRef
8.
go back to reference Rasul S, Ilhan A, Wagner I, Luger A, Kautzky-Willer A (2012) Diabetic polyneuropathy relates to bone metabolism and markers of bone turnover in elderly patients with type 2 diabetes: Greater Effects in Male Patients. Gender Medicine. 9(3):187–196CrossRefPubMedCentral Rasul S, Ilhan A, Wagner I, Luger A, Kautzky-Willer A (2012) Diabetic polyneuropathy relates to bone metabolism and markers of bone turnover in elderly patients with type 2 diabetes: Greater Effects in Male Patients. Gender Medicine. 9(3):187–196CrossRefPubMedCentral
9.
go back to reference Beeve AT, Brazill JM, Scheller EL (2019) Peripheral neuropathy as a component of skeletal disease in diabetes. Curr Osteoporos Rep 17:256–269CrossRefPubMedCentral Beeve AT, Brazill JM, Scheller EL (2019) Peripheral neuropathy as a component of skeletal disease in diabetes. Curr Osteoporos Rep 17:256–269CrossRefPubMedCentral
10.
go back to reference Castrogiovanni P, Trovato FM, Szychlinska MA, Nsir H, Imbesi R, Musumeci G (2016) The importance of physical activity in osteoporosis. From the molecular pathways to the clinical evidence. Histol Histopathol. 31(11):1183–1194PubMed Castrogiovanni P, Trovato FM, Szychlinska MA, Nsir H, Imbesi R, Musumeci G (2016) The importance of physical activity in osteoporosis. From the molecular pathways to the clinical evidence. Histol Histopathol. 31(11):1183–1194PubMed
11.
go back to reference Tennant F and Hermann L. (2001) (229) Serum cortisol concentrations and adrenal reserve may be altered by severe chronic pain. Pain Med. 2(3): 252 Tennant F and Hermann L. (2001) (229) Serum cortisol concentrations and adrenal reserve may be altered by severe chronic pain. Pain Med. 2(3): 252
12.
go back to reference Okada Y, Tanaka Y (2004) Immune signals in the context of secondary osteoporosis. Histol Histopathol. 19(3):863–866PubMed Okada Y, Tanaka Y (2004) Immune signals in the context of secondary osteoporosis. Histol Histopathol. 19(3):863–866PubMed
13.
go back to reference Bouhassira D, Attal N, Alchaar H, Boureau F, Brochet B, Bruxelle J, Cunin G, Fermanian J, Ginies P, Grun-Overdyking A, Jafari-Schluep H, Lantéri-Minet M, Laurent B, Mick G, Serrie A, Valade D, Vicaut E (2005) Comparison of pain syndromes associated with nervous or somatic lesions and development of a new neuropathic pain diagnostic questionnaire (DN4). Pain. 114(1-2):29–36CrossRef Bouhassira D, Attal N, Alchaar H, Boureau F, Brochet B, Bruxelle J, Cunin G, Fermanian J, Ginies P, Grun-Overdyking A, Jafari-Schluep H, Lantéri-Minet M, Laurent B, Mick G, Serrie A, Valade D, Vicaut E (2005) Comparison of pain syndromes associated with nervous or somatic lesions and development of a new neuropathic pain diagnostic questionnaire (DN4). Pain. 114(1-2):29–36CrossRef
14.
go back to reference Unal-Cevik I, Sarioglu-Ay S, Evcik D (2010) A comparison of the DN4 and LANSS questionnaires in the assessment of neuropathic pain: validity and reliability of the Turkish version of DN4. The Journal of Pain. 11(11):1129–1135CrossRef Unal-Cevik I, Sarioglu-Ay S, Evcik D (2010) A comparison of the DN4 and LANSS questionnaires in the assessment of neuropathic pain: validity and reliability of the Turkish version of DN4. The Journal of Pain. 11(11):1129–1135CrossRef
15.
go back to reference Spallone V, Morganti R, D’Amato C, Greco C, Cacciotti L, Marfia GA (2012) Validation of DN4 as a screening tool for neuropathic pain in painful diabetic polyneuropathy. Diabet Med 29:578–585CrossRef Spallone V, Morganti R, D’Amato C, Greco C, Cacciotti L, Marfia GA (2012) Validation of DN4 as a screening tool for neuropathic pain in painful diabetic polyneuropathy. Diabet Med 29:578–585CrossRef
16.
go back to reference World Health Organization. (2007) WHO scientific group on the assessment of osteoporosis at the primary health care level: summary meeting report. Brussels, Belgium; May 5–7 (2004) Geneva. World Health Organization, Switzerland World Health Organization. (2007) WHO scientific group on the assessment of osteoporosis at the primary health care level: summary meeting report. Brussels, Belgium; May 5–7 (2004) Geneva. World Health Organization, Switzerland
17.
go back to reference Jeffcoate W (2004) Vascular calcification and osteolysis in diabetic neuropathy—is RANK-L the missing link? Diabetologia. 47(9):1488–1492CrossRef Jeffcoate W (2004) Vascular calcification and osteolysis in diabetic neuropathy—is RANK-L the missing link? Diabetologia. 47(9):1488–1492CrossRef
18.
go back to reference Kluding PM, Bareiss SK, Hastings M, Marcus RL, Sinacore DR, Mueller MJ (2017) Physical training and activity in people with diabetic peripheral neuropathy: paradigm shift. Phys Ther. 97(1):31–43PubMed Kluding PM, Bareiss SK, Hastings M, Marcus RL, Sinacore DR, Mueller MJ (2017) Physical training and activity in people with diabetic peripheral neuropathy: paradigm shift. Phys Ther. 97(1):31–43PubMed
19.
go back to reference Woolf CJ, Mannion RJ (1999) Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet. 353(9168):1959–1964CrossRef Woolf CJ, Mannion RJ (1999) Neuropathic pain: aetiology, symptoms, mechanisms, and management. Lancet. 353(9168):1959–1964CrossRef
20.
21.
go back to reference Sorensen L, Molyneaux L, Yue DK (2006) The relationship among pain, sensory loss, and small nerve fibers in diabetes. Diabetes Care. 29:883–887CrossRefPubMedCentral Sorensen L, Molyneaux L, Yue DK (2006) The relationship among pain, sensory loss, and small nerve fibers in diabetes. Diabetes Care. 29:883–887CrossRefPubMedCentral
22.
go back to reference Young RJ, Zhou YQ, Rodriguez E, Prescott RJ, Ewing DJ, Clarke BF (1986) Variable relationship between peripheral somatic and autonomic neuropathy in patients with different syndromes of diabetic polyneuropathy. Diabetes. 35:192–197CrossRefPubMedCentral Young RJ, Zhou YQ, Rodriguez E, Prescott RJ, Ewing DJ, Clarke BF (1986) Variable relationship between peripheral somatic and autonomic neuropathy in patients with different syndromes of diabetic polyneuropathy. Diabetes. 35:192–197CrossRefPubMedCentral
24.
go back to reference Doupis J, Lyons TE, Wu S, Gnardellis C, Dinh T, Veves A (2009) Microvascular reactivity and inflammatory cytokines in painful and painless peripheral diabetic neuropathy. J Clin Endocrinol Metab. 94(6):2157–2163CrossRefPubMedCentral Doupis J, Lyons TE, Wu S, Gnardellis C, Dinh T, Veves A (2009) Microvascular reactivity and inflammatory cytokines in painful and painless peripheral diabetic neuropathy. J Clin Endocrinol Metab. 94(6):2157–2163CrossRefPubMedCentral
25.
go back to reference Cauley JA, Danielson ME, Boudreau RM, YZ. Forrest YZ, Zmuda JM, Pahor M, et al (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res. 22(7): 1088-1095. Cauley JA, Danielson ME, Boudreau RM, YZ. Forrest YZ, Zmuda JM, Pahor M, et al (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res. 22(7): 1088-1095.
26.
go back to reference Barbour KE, Lui LY, Ensrud KE, Hillier TA, LeBlanc ES, Ing SW et al (2014) Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Miner Res. 29(9):2057–2064CrossRefPubMedCentral Barbour KE, Lui LY, Ensrud KE, Hillier TA, LeBlanc ES, Ing SW et al (2014) Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Miner Res. 29(9):2057–2064CrossRefPubMedCentral
27.
go back to reference Tennant F (2012) Cortisol screening in chronic pain patients. Pract Pain Manage. 12(1):43–47 Tennant F (2012) Cortisol screening in chronic pain patients. Pract Pain Manage. 12(1):43–47
28.
go back to reference Wacker M, Holick MF (2013) Vitamin D - effects on skeletal and extraskeletal health and the need for supplementation. Nutrients. 5(1):111–148CrossRefPubMedCentral Wacker M, Holick MF (2013) Vitamin D - effects on skeletal and extraskeletal health and the need for supplementation. Nutrients. 5(1):111–148CrossRefPubMedCentral
29.
go back to reference Sari A, Akdoğan Altun Z, Arifoglu Karaman C, Bilir Kaya B, Durmus B (2020) Does vitamin D affect diabetic neuropathic pain and balance? J Pain Res. 13:171–179CrossRefPubMedCentral Sari A, Akdoğan Altun Z, Arifoglu Karaman C, Bilir Kaya B, Durmus B (2020) Does vitamin D affect diabetic neuropathic pain and balance? J Pain Res. 13:171–179CrossRefPubMedCentral
30.
go back to reference Basit A, Basit KA, Fawwad A, Shaheen F, Fatima N, Petropoulos IN, Alam U, Malik RA (2016) Vitamin D for the treatment of painful diabetic neuropathy. BMJ Open Diabetes Res Care. 4(1):e000148CrossRefPubMedCentral Basit A, Basit KA, Fawwad A, Shaheen F, Fatima N, Petropoulos IN, Alam U, Malik RA (2016) Vitamin D for the treatment of painful diabetic neuropathy. BMJ Open Diabetes Res Care. 4(1):e000148CrossRefPubMedCentral
31.
go back to reference Basantsova NY, Starshinova AA, Dori A, Zinchenko YS, Yablonskiy PK, Shoenfeld Y (2019) Small-fiber neuropathy definition, diagnosis, and treatment. Neurol Sci 40:1343–1350CrossRef Basantsova NY, Starshinova AA, Dori A, Zinchenko YS, Yablonskiy PK, Shoenfeld Y (2019) Small-fiber neuropathy definition, diagnosis, and treatment. Neurol Sci 40:1343–1350CrossRef
Metadata
Title
The increase of neuropathic symptoms in diabetic patients is related with osteopenia
Authors
Elif Börekci
Adem Kara
Mahmut Kılıç
Nermin Tanık
Zeynep T. Ozan
Tekin Yıldırım
Yalçın Aral
Publication date
01-07-2021
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 7/2021
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04915-3

Other articles of this Issue 7/2021

Neurological Sciences 7/2021 Go to the issue