DOI QR코드

DOI QR Code

Development of a Diabetic Foot Ulceration Prediction Model and Nomogram

당뇨병성 발궤양 발생 위험 예측모형과 노모그램 개발

  • Lee, Eun Joo (College of Nursing, Healthcare Sciences & Human Ecology, Dong-Eui University) ;
  • Jeong, Ihn Sook (College of Nursing, Pusan National University) ;
  • Woo, Seung Hun (Department of Orthopedics, Pusan National University Yangsan Hospital) ;
  • Jung, Hyuk Jae (Endovascular and Vascular and Transplantation Division, Department of Surgery, Pusan National University Hospital) ;
  • Han, Eun Jin (Division of Nursing, Severance Hospital) ;
  • Kang, Chang Wan (IT Convergence College of Components and Materials Engineering, Dong-Eui University) ;
  • Hyun, Sookyung (College of Nursing, Pusan National University)
  • 이은주 (동의대학교 의료보건생활대학) ;
  • 정인숙 (부산대학교 간호대학) ;
  • 우승훈 (양산부산대학교병원 정형외과) ;
  • 정혁재 (부산대학교병원 혈관이식외과) ;
  • 한은진 (세브란스병원 간호국) ;
  • 강창완 (동의대학교 IT융합부품소재공과대학) ;
  • 현수경 (부산대학교 간호대학)
  • Received : 2020.10.28
  • Accepted : 2021.03.15
  • Published : 2021.06.30

Abstract

Purpose: This study aimed to identify the risk factors for diabetic foot ulceration (DFU) to develop and evaluate the performance of a DFU prediction model and nomogram among people with diabetes mellitus (DM). Methods: This unmatched case-control study was conducted with 379 adult patients (118 patients with DM and 261 controls) from four general hospitals in South Korea. Data were collected through a structured questionnaire, foot examination, and review of patients' electronic health records. Multiple logistic regression analysis was performed to build the DFU prediction model and nomogram. Further, their performance was analyzed using the Lemeshow-Hosmer test, concordance statistic (C-statistic), and sensitivity/specificity analyses in training and test samples. Results: The prediction model was based on risk factors including previous foot ulcer or amputation, peripheral vascular disease, peripheral neuropathy, current smoking, and chronic kidney disease. The calibration of the DFU nomogram was appropriate (χ2 = 5.85, p = .321). The C-statistic of the DFU nomogram was .95 (95% confidence interval .93~.97) for both the training and test samples. For clinical usefulness, the sensitivity and specificity obtained were 88.5% and 85.7%, respectively at 110 points in the training sample. The performance of the nomogram was better in male patients or those having DM for more than 10 years. Conclusion: The nomogram of the DFU prediction model shows good performance, and is thereby recommended for monitoring the risk of DFU and preventing the occurrence of DFU in people with DM.

Keywords

Acknowledgement

The authors express special thanks to Dr. R. Garry Sibbald for kindly giving us his permission to use the 60-second tool.

References

  1. World Health Organization (WHO). Global report on diabetes [Internet]. Geneva: World Health Organization; c2016 [cited 2016 Apr 8]. Available from: http://www.who.int/diabetes/publications/grd-2016/en.
  2. International Diabetes Federation (IDF). IDF diabetes atlas [Internet]. Brussels: International Diabetes Federation; c2019 [cited 2020 Jul 14]. Available from: https://www.diabetesatlas.org/en/.
  3. Korean Diabetes Association (KDA). Diabetes fact sheet in Korea 2018 [Internet]. Seoul: Korean Diabetes Association; c2018 [cited 2020 Jul 19]. Available from: https://www.diabetes.or.kr/pro.
  4. National Institute for Health and Care Excellence (NICE). Diabetic foot problems: Prevention and management [Internet]. London: National Institute for Health and Care Excellence; c2015 [cited 2017 Mar 11]. Available from: https://www.nice.org.uk/guidance/ng19.
  5. Suh HS, Hong JP. Diabetic foot ulcer. Journal of the Korean Medical Association. 2015;58(9):795-800. https://doi.org/10.5124/jkma.2015.58.9.795
  6. Zhang P, Lu J, Jing Y, Tang S, Zhu D, Bi Y. Global epidemiology of diabetic foot ulceration: A systematic review and meta-analysis. Annals of Medicine. 2017;49(2):106-116. https://doi.org/10.1080/07853890.2016.1231932
  7. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, et al. High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study. Diabetologia. 2007;50(1):18-25. https://doi.org/10.1007/s00125-006-0491-1
  8. Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. The Lancet. 2005;366(9498):1719-1724. https://doi.org/10.1016/S0140-6736(05)67698-2
  9. Armstrong DG, Boulton AJM, Bus SA. Diabetic foot ulcers and their recurrence. The New England Journal of Medicine. 2017;376(24):2367-2375. https://doi.org/10.1056/NEJMra1615439
  10. Boulton AJ, Armstrong DG, Albert SF, Frykberg RG, Hellman R, Kirkman MS, et al. Comprehensive foot examination and risk assessment: A report of the task force of the foot care interest group of the American Diabetes Association, with endorsement by the American Association of Clinical Endocrinologists. Diabetes Care. 2008;31(8):1679-1685. https://doi.org/10.2337/dc08-9021
  11. Schaper NC, van Netten JJ, Apelqvist J, Bus SA, Hinchliffe RJ, Lipsky BA. Practical Guidelines on the prevention and management of diabetic foot disease (IWGDF 2019 update). Diabetes/Metabolism Research and Reviews. 2020;36 Suppl 1:e3266. https://doi.org/10.1002/dmrr.3266
  12. Crawford F, Cezard G, Chappell FM, Murray GD, Price JF, Sheikh A, et al. A systematic review and individual patient data meta-analysis of prognostic factors for foot ulceration in people with diabetes: The international research collaboration for the prediction of diabetic foot ulcerations (PODUS). Health Technology Assessment. 2015;19(57):1-210. https://doi.org/10.3310/hta19570
  13. Monteiro-Soares M, Boyko EJ, Ribeiro J, Ribeiro I, Dinis-Ribeiro M. Predictive factors for diabetic foot ulceration: A systematic review. Diabetes/Metabolism Research and Reviews. 2012;28(7):574-600. https://doi.org/10.1002/dmrr.2319
  14. Park SA, Ko SH, Lee SH, Cho JH, Moon SD, Jang SA, et al. Incidence of diabetic foot and associated risk factors in type 2 diabetic patients: A five-year observational study. Korean Diabetes Journal. 2009;33(4):315-323. https://doi.org/10.4093/kdj.2009.33.4.315
  15. Boyko EJ, Ahroni JH, Cohen V, Nelson KM, Heagerty PJ. Prediction of diabetic foot ulcer occurrence using commonly available clinical information: The Seattle Diabetic Foot Study. Diabetes Care. 2006;29(6):1202-1207. https://doi.org/10.2337/dc05-2031
  16. Korean Diabetes Association. Treatment guideline for diabetes. 6th ed. Seoul: Korean Diabetes Association; 2019. p. 122.
  17. Park IB, Kim J, Kim DJ, Chung CH, Oh JY, Park SW, et al. Diabetes epidemics in Korea: Reappraise nationwide survey of diabetes "Diabetes in Korea 2007". Diabetes and Metabolism Journal. 2013;37(4):233-239. https://doi.org/10.4093/dmj.2013.37.4.233
  18. Iasonos A, Schrag D, Raj GV, Panageas KS. How to build and interpret a nomogram for cancer prognosis. Journal of Clinical Oncology. 2008;26(8):1364-1370. https://doi.org/10.1200/JCO.2007.12.9791
  19. Balachandran VP, Gonen M, Smith JJ, DeMatteo RP. Nomograms in oncology: More than meets the eye. The Lancet. Oncology. 2015;16(4):e173-e180. https://doi.org/10.1016/S1470-2045(14)71116-7
  20. Chung SM, Park JC, Moon JS, Lee JY. Novel nomogram for screening the risk of developing diabetes in a Korean population. Diabetes Research and Clinical Practice. 2018;142:286-293. https://doi.org/10.1016/j.diabres.2018.05.036
  21. Lee EJ, Jeong IS, Kim IJ, Cho, YH, Kim YJ. Distribution of risk factors and risk classification of diabetic foot ulcer. Paper presented at: Nursing challenges and opportunities in rapidly changing healthcare. 2017 PNU International Nursing Conference of the Research Institute of Nursing Science; 2017 Jun 28; Yangsan, Korea.
  22. Dean AG, Sullivan KM, Soe MM. OpenEpi: Open source epidemiologic statistics for public health, version 3.01 [Internet]. OpenEpi; c2013 [cited 2017 Apr 19]. Available from: http://www.openepi.com.
  23. Baba M, Davis WA, Davis TM. A longitudinal study of foot ulceration and its risk factors in community-based patients with type 2 diabetes: The Fremantle Diabetes Study. Diabetes Research and Clinical Practice. 2014;106(1):42-49. https://doi.org/10.1016/j.diabres.2014.07.021
  24. Gordis L. Epidemiology. 5th ed. Philadelphia (PA): Elsevier Saunders; 2013. p. 201.
  25. Bleeker SE, Moll HA, Steyerberg EW, Donders AR, Derksen-Lubsen G, Grobbee DE, et al. External validation is necessary in prediction research: A clinical example. Journal of Clinical Epidemiology. 2003;56(9):826-832. https://doi.org/10.1016/s0895-4356(03)00207-5
  26. Debray TP, Vergouwe Y, Koffijberg H, Nieboer D, Steyerberg EW, Moons KG. A new framework to enhance the interpretation of external validation studies of clinical prediction models. Journal of Clinical Epidemiology. 2015;68(3):279-289. https://doi.org/10.1016/j.jclinepi.2014.06.018
  27. Dobbin KK, Simon RM. Optimally splitting cases for training and testing high dimensional classifiers. BMC Medical Genomics. 2011;4:31. https://doi.org/10.1186/1755-8794-4-31
  28. Sibbald RG, Ayello EA, Alavi A, Ostrow B, Lowe J, Botros M, et al. Screening for the high-risk diabetic foot: A 60-second tool (2012). Advances in Skin & Wound Care. 2012;25(10):465-476. https://doi.org/10.1097/01.ASW.0000421460.21773.7b
  29. Hurley L, Kelly L, Garrow AP, Glynn LG, McIntosh C, Alvarez-Iglesias A, et al. A prospective study of risk factors for foot ulceration: The West of Ireland Diabetes Foot Study. QJM. 2013;106(12):1103-1110. https://doi.org/10.1093/qjmed/hct182
  30. Korea Centers for Disease Control and Prevention (KCDC). Korea health statistics 2018: Korea National Health and Nutrition Examination Survey (KNHANES VII-3) [Internet]. Sejong: Ministry of Health and Welfare; c2019 [cited 2020 Jul 19]. Available from: https://knhanes.kdca.go.kr/knhanes/sub04/sub04_04_01.do.
  31. National Institute for Health and Care Excellence (NICE). Type 2 diabetes in adults: Management [Internet]. London: National Institute for Health and Care Excellence; c2015 [cited 2016 Aug 1]. Available from: https://www.nice.org.uk/guidance/ng28/resources/type-2-diabetes-inadults-2830067254213.
  32. Registered Nurses' Association of Ontario (RNAO). Assessment and management of foot ulcers for people with diabetes. 2nd ed. [Internet]. Toronto: Registered Nurses' Association of Ontario; c2013 [cited 2017 Oct 14]. Available from: https://rnao.ca/bpg/guidelines/assessment-and-management-foot-ulcers-people-diabetes-second-edition.
  33. Steyerberg EW, Vergouwe Y. Towards better clinical prediction models: Seven steps for development and an ABCD for validation. European Heart Journal. 2014;35(29):1925-1931. https://doi.org/10.1093/eurheartj/ehu207
  34. Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143(1):29-36. https://doi.org/10.1148/radiology.143.1.7063747
  35. Scottish Intercollegiate Guidelines Network (SIGN). Management of diabetes: A national clinical guideline [Internet]. Edinburgh: Scottish Intercollegiate Guidelines Network; c2010 [cited 2017 Mar 11]. Available from: https://www.sign.ac.uk/media/1054/sign116.pdf.
  36. Jiang Y, Wang X, Xia L, Fu X, Xu Z, Ran X, et al. A cohort study of diabetic patients and diabetic foot ulceration patients in China. Wound Repair and Regeneration. 2015;23(2):222-230. https://doi.org/10.1111/wrr.12263
  37. Bruun C, Siersma V, Guassora AD, Holstein P, de Fine Olivarius N. Amputations and foot ulcers in patients newly diagnosed with type 2 diabetes mellitus and observed for 19 years. The role of age, gender and co-morbidity. Diabetic Medicine. 2013;30(8):964-972. https://doi.org/10.1111/dme.12196
  38. Monteiro-Soares M, Dinis-Ribeiro M. External validation and optimisation of a model for predicting foot ulcers in patients with diabetes. Diabetologia. 2010;53(7):1525-1533. https://doi.org/10.1007/s00125-010-1731-y
  39. Akobeng AK. Understanding diagnostic tests 1: Sensitivity, specificity and predictive values. Acta Paediatrica. 2007;96(3):338-341. https://doi.org/10.1111/j.1651-2227.2006.00180.x
  40. Parikh R, Mathai A, Parikh S, Chandra Sekhar G, Thomas R. Understanding and using sensitivity, specificity and predictive values. Indian Journal of Ophthalmology. 2008;56(1):45-50. https://doi.org/10.4103/0301-4738.37595
  41. Paisey RB, Darby T, George AM, Waterson M, Hewson P, Paisey CF, et al. Prediction of protective sensory loss, neuropathy and foot ulceration in type 2 diabetes. BMJ Open Diabetes Research & Care. 2016;4(1):e000163. https://doi.org/10.1136/bmjdrc-2015-000163
  42. Al-Rubeaan K, Al Derwish M, Ouizi S, Youssef AM, Subhani SN, Ibrahim HM, et al. Diabetic foot complications and their risk factors from a large retrospective cohort study. PLoS One. 2015;10(5):e0124446. https://doi.org/10.1371/journal.pone.0124446