ORIGINAL PAPER
Contribution of infection and peripheral artery disease to severity of diabetic foot ulcers in Chinese patients D. Hao,1,* C. Hu,2,* T. Zhang,3,* G. Feng,1 J. Chai,1 T. Li1
1
SUMMARY
What’s known
Aim: The objective of the current ongoing study was to evaluate the characteristics of diabetic patients with newly diagnosed foot ulcer in Burn & Plastic Hospital of PLA General Hospital. Methods: A total of 1002 consecutive patients presenting with a new foot ulcer between March 2007 and September 2013 were enrolled. All enrolled patients were classified based on presence or absence of collateral infection, disabling comorbidities and peripheral arterial disease (PAD). Results: Of patients, 70.05% had PAD, which occurred significantly more in elderly adults. Patients with PAD had higher incidence of infection (58.9% vs. 41.5% in non-PAD group) and disabling comorbidities (79% in PAD and 61% in non-PAD; p < 0.038). There was no significant difference observed in depth, size and duration of foot ulcers between the PAD and non-PAD group of enrolled diabetic patients. Conclusions: Diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity.
Introduction The incidence rate of foot ulcer in diabetes patients is one in seven, with a high proportion requiring prolonged treatment, hospitalisation and amputation (1,2). Foot ulcers can result from a multitude of factors, inclusive of peripheral arterial disease (PAD), external trauma, and excessive and abnormal biomechanical stress, and can be further compounded by infection (3,4). Taking into account the cost of healthcare burden of foot ulcers in diabetic patients and to the healthcare system at large, it has been realised that more pro-active research and treatment strategies are required to tackle the condition (5,6). It is currently appreciated that treatment and management strategies for foot ulcers will be dictated by the underlying cause and the presence of comorbidities, like diabetes (1,7). Multicentre studies incorporating large patient cohort are lacking, except for the European Study Group on Diabetes and the Lower Extremity (EURODIALE) (8), are severely lacking, especially in China; however, the significance ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164. doi: 10.1111/ijcp.12440
•
• •
The incidence rate of foot ulcer in diabetes patients is one in seven, with a high proportion requiring prolonged treatment, hospitalisation and amputation. Foot ulcers can result from a multitude of factors, inclusive of peripheral arterial disease (PAD). Multicentre studies incorporating large patient cohort are lacking in China.
What’s new
•
•
Diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity. Follow-up data on these patients, which will be completed in September 2014, will perhaps give us more insight into the implications of the severity of this disease for clinical outcome, resource utilisation and finally, quality of life.
of patient characteristics and comorbidities have been highlighted in a few studies (1,9–11). Of note, the observed differences between patient characteristics, comorbidities, and occurrence and outcome of foot ulcer can be dictated by demographics, race and the referral system followed in a particular region or nation (1,9,12–16). Hence, the objective of this study, in keeping with the EURODIALE study (8), was to acquire data on clinical outcome (healing rate, healing time, amputation and death) in newly diagnosed foot ulcer patients with different disease severity and ulcer phenotypes. Presented here are the initial observations from the baseline observation of the enrolled patients.
Department of Burn & Plastic Surgery, Burns Institute, Burn & Plastic Hospital of Chinese PLA General Hospital, Beijing, China 2 Beijing Luhe Hospital, Capital Medical University, Beijing, China 3 Central Hospital of Qilu Petrochemical Hospital Corporation, Shandong, China Correspondence to: Daifeng Hao, Department of Burn & Plastic Surgery, Burns Institute, Burn & Plastic Hospital of PLA General Hospital, No. 51 Fucheng Road, Haidian District, Beijing 100048, China Tel.: +86-10-010-66867972 Fax: +86-10-010-68989181 Email: haodaifeng304@163. com
*These authors contributed equally to this work. Disclosure The authors do not have any conflict of interest, financial or otherwise, to report.
Methods Study design, inclusion and exclusion criteria This study was approved by the Institutional Review Board of the Burn & Plastic Hospital of PLA General Hospital, Beijing, China. One thousand and two consecutive diabetic patients (inclusive of in- and outpatients) presenting with a new foot ulcer between
1161
1162
Contribution of infection and peripheral artery disease
March 2007 and September 2013 were consented to participate in the study. A full-thickness lesion below the ankle was defined as a bona fide foot ulcer (17). Patients who were treated on the same foot for foot ulcer within the last year were excluded from this study. Patients were followed up at intervals of 1 month up to 1 year or complete healing or major amputation, whichever was earlier.
Data collection Data were recorded at onset of participation and during each follow up on standardised case record forms. Focus was made to collect information pertaining to individual (haemoglobin A1c (HbA1c), and serum creatinine levels, comorbidity, previous management and general living conditions) and disease-specific factors that might influence overall management strategies and ultimate outcome. Severe visual impairment (vision 6/24 to 6/60), end-stage renal disease, heart failure and/or angina pectoris (New York Heart Association stage III or IV) and inability to stand or walk without support were classified as disabling comorbidities. The perfusion-extent-depth-infection-sensation system was used to classify the foot ulcers (17,18). An ankle-brachial pressure index (ABPI) of 1.2 and hence not convincing. PAD occurred more frequently in older patients (in 71% of patients aged > 70 years). Disabling comorbidity, other than infection, was present in 79 (severe visual impairment – 33%; end-stage renal disease – 16%; heart failure – 18%; inability to stand or walk – 12%) and 61% (severe visual impairment – 28%;
Table 1 General baseline characteristics of the enrolled patients based on associated peripheral arterial disease (PAD)
Characteristic
Patients with PAD (n = 702)
Age (years) 65 12 Men, n (%) 450 (64.1) Duration of diabetes (%) < 5 years 11.3 5–10 years 13.6 > 10 years 75.1 Deep ulcer (%) 53.2 Size of ulcer (%) < 1 cm2 33.2 1–5 cm2 54.9 > 5 cm2 11.9 Duration of ulcer (%) < 1 week 8.9 1 week–3 months 49.3 > 3 months 41.8 69.3 Glycosylated haemoglobin > 8.4 (%) 79 Disabling comorbidity, other than infection (%) Infection (%) 58.9
Patients without PAD (n = 300)
p-value
58.7 3 197 (65.6)
< 0.001 0.564
12.1 15.3 72.6 48.1
0.487
34.9 52.3 12.8
0.107
9.3 46.5 44.2 53.4
0.149
61
0.038
41.5
< 0.001
0.239
0.006
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
Contribution of infection and peripheral artery disease
end-stage renal disease – 14%; heart failure – 10%; inability to stand or walk – 9%) of diabetic patients with and without PAD, respectively. The percentage of infection in PAD patients (58.9%) was significantly higher than in patients without PAD (41.5%) (p < 0.001). However, there was no difference between the PAD and non-PAD groups in duration of diabetes and depth, severity, or duration of ulcer
Discussion We have presented data on disease severity at presentation and the relationship with patient characteristics in a cross-section of patients with diabetic foot ulcer treated in our hospital between March 2007 and September 2013. Data were obtained in 1002 diabetic patients with a new ulcer and baseline data of enrolled patients are presented here. One of the strengths of this study is that it reflects daily clinical practice. Some of our initial findings are similar to those observed in the now completed EURODIALE study (8), especially that a large per cent of enrolled patients had severe disease with co-occurrence of PAD and infection. However, as opposed to the EURODIALE study, this study did not reveal any significant difference in depth, size and duration of ulcer; of note though our study is still ongoing and the final numbers might see some variation once the final analyses are completed at the conclusion of the study in September 2014. It has been previously shown that the prevalence of PAD varied between 10% and 60% (19–22); however, in this study we saw PAD incidence in 70.05% patients, higher than what had been previously reported. However, it must be noted that the degree of peripheral ischaemia can vary substantially between patients and, unfortunately, physical exami-
References 1 Reiber GE, Vileikyte L, Boyko EJ et al. Causal pathways for incident lower-extremity ulcers in patients with diabetes from two settings. Diabetes Care 1999; 22: 157–62. 2 Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet 2003; 361: 1545–51. 3 Boulton AJ. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia 2004; 47: 1343–53. 4 Reiber GE, Lipsky BA, Gibbons GW. The burden of diabetic foot ulcers. Am J Surg 1998; 176: 5S–10S. 5 Ragnarson Tennvall G, Apelqvist J. Health–economic consequences of diabetic foot lesions. Clin Infect Dis 2004; 39(S2): S132–9. 6 Frykberg RG. An evidence-based approach to diabetic foot infections. Am J Surg 2003; 186: 44S– 54S; discussion 61S–64S. 7 Apelqvist J, Agardh CD. The association between clinical risk factors and outcome of diabetic foot ulcers. Diabetes Res Clin Pract 1992; 18: 43–53. ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
1163
nation is of limited value in resolving such disputes (23). For example, whereas in non-diabetic patients ABPI measurement is an accurate indicator of PAD, in diabetic patients it is not, partly because of noncompressibility of lower limb arteries (23). Indeed, in our study, non-compressible lower leg arteries, with an ABPI of > 1.2 were observed in 43% of the patients. Of note though, as ABPI < 0.9 are indicative of PAD both in non-diabetic and diabetic patients, we are confident that these patients were correctly categorised as having PAD. We also found a relatively high prevalence of infection in patients with PAD (58.9%) as compared with the non-PAD group of patients (41.5%). Our finding of coexistence of infection and PAD corroborates previous findings (9,19,20). It would be interesting to determine at the end of this study whether PAD and infection combination is also associated with the worst outcome among patients, as was observed in the EURODIALE study (8). Our study does have some potential limitations stemming from the fact that is a hospital-based observational study evaluating consecutive patients and diabetic foot ulceration is a recurrent disease (24,25). Furthermore, since patients with an ulcer within the last year were excluded from this study, our patient population is not an exact reflection of the entire population. In conclusion, diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity. Followup data on these patients, which will be completed in September 2014, will perhaps give us more insight into the implications of the severity of this disease for clinical outcome, resource utilisation and finally, quality of life.
8 Prompers L, Schaper N, Apelqvist J et al. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study. Diabetologia 2008; 51: 747–55. 9 Armstrong DG, Lavery LA, Harkless LB. Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 1998; 21: 855–9. 10 Ramsey SD, Newton K, Blough D et al. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999; 22: 382–7. 11 Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: the association of wound size, wound duration, and wound grade on healing. Diabetes Care 2002; 25: 1835–9. 12 Mueller MJ, Sinacore DR, Hastings MK, Strube MJ, Johnson JE. Effect of Achilles tendon lengthening on neuropathic plantar ulcers. A randomized clinical trial. J Bone Joint Surg Am 2003; 85-A: 1436–45.
13 Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ. Predictive value of foot pressure assessment as part of a population-based diabetes disease management program. Diabetes Care 2003; 26: 1069–73. 14 Nabuurs-Franssen MH, Sleegers R, Huijberts MS et al. Total contact casting of the diabetic foot in daily practice: a prospective follow up study. Diabetes Care 2005; 28: 243–7. 15 Mueller MJ, Diamond JE, Sinacore DR et al. Total-contact casting in treatment of diabetic plantar ulcers. Controlled clinical trial. Diabetes Care 1989; 12: 384–8. 16 Armstrong DG, Nguyen HC, Lavery LA, van Schie CH, Boulton AJ, Harkless LB. Off-loading the diabetic foot wound: a randomized clinical trial. Diabetes Care 2001; 24: 1019–22. 17 Schaper NC. Diabetic foot ulcer classification system for research purposes: a progress report on criteria for including patients in research studies. Diabetes Metab Res Rev 2004; 20(S1): S90–5.
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Contribution of infection and peripheral artery disease
18 Boulton AJ, Gries FA, Jervell JA. Guidelines for the diagnosis and outpatient management of diabetic peripheral neuropathy. Diabet Med 1998; 15: 508– 14. 19 Oyibo SO, Jude EB, Tarawneh I et al. The effects of ulcer size and site, patient’s age, sex and type and duration of diabetes on the outcome of diabetic foot ulcers. Diabet Med 2001; 18: 133–8. 20 Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ. A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care 2001; 24: 84–8.
21 Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic foot ulcers stratified by etiology. Diabetes Care 2003; 26: 491–4. 22 Apelqvist J, Larsson J, Agardh CD. The importance of peripheral pulses, peripheral oedema and local pain for the outcome of diabetic foot ulcers. Diabet Med 1990; 7: 590–4. 23 Schaper NC, Nabuurs-Franssen MH. The diabetic foot: pathogenesis and clinical evaluation. Semin Vasc Med 2002; 2: 221–8. 24 Lipsky BA, Armstrong DG, Citron DM, Tice AD, Morgenstern DE, Abramson MA. Ertapenem versus piperacillin/tazobactam for diabetic foot infections
(SIDESTEP): prospective, randomised, controlled, double-blinded, multicentre trial. Lancet 2005; 366: 1695–703. 25 Abbott CA, Carrington AL, Ashe H et al.; North-West Diabetes Foot Care Study. The North-West Diabetes Foot Care Study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med 2002; 19: 377–84.
Paper received October 2013, accepted March 2014
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
Contribution of infection and peripheral artery disease to severity of diabetic foot ulcers in Chinese patients D. Hao,1,* C. Hu,2,* T. Zhang,3,* G. Feng,1 J. Chai,1 T. Li1
1
SUMMARY
What’s known
Aim: The objective of the current ongoing study was to evaluate the characteristics of diabetic patients with newly diagnosed foot ulcer in Burn & Plastic Hospital of PLA General Hospital. Methods: A total of 1002 consecutive patients presenting with a new foot ulcer between March 2007 and September 2013 were enrolled. All enrolled patients were classified based on presence or absence of collateral infection, disabling comorbidities and peripheral arterial disease (PAD). Results: Of patients, 70.05% had PAD, which occurred significantly more in elderly adults. Patients with PAD had higher incidence of infection (58.9% vs. 41.5% in non-PAD group) and disabling comorbidities (79% in PAD and 61% in non-PAD; p < 0.038). There was no significant difference observed in depth, size and duration of foot ulcers between the PAD and non-PAD group of enrolled diabetic patients. Conclusions: Diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity.
Introduction The incidence rate of foot ulcer in diabetes patients is one in seven, with a high proportion requiring prolonged treatment, hospitalisation and amputation (1,2). Foot ulcers can result from a multitude of factors, inclusive of peripheral arterial disease (PAD), external trauma, and excessive and abnormal biomechanical stress, and can be further compounded by infection (3,4). Taking into account the cost of healthcare burden of foot ulcers in diabetic patients and to the healthcare system at large, it has been realised that more pro-active research and treatment strategies are required to tackle the condition (5,6). It is currently appreciated that treatment and management strategies for foot ulcers will be dictated by the underlying cause and the presence of comorbidities, like diabetes (1,7). Multicentre studies incorporating large patient cohort are lacking, except for the European Study Group on Diabetes and the Lower Extremity (EURODIALE) (8), are severely lacking, especially in China; however, the significance ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164. doi: 10.1111/ijcp.12440
•
• •
The incidence rate of foot ulcer in diabetes patients is one in seven, with a high proportion requiring prolonged treatment, hospitalisation and amputation. Foot ulcers can result from a multitude of factors, inclusive of peripheral arterial disease (PAD). Multicentre studies incorporating large patient cohort are lacking in China.
What’s new
•
•
Diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity. Follow-up data on these patients, which will be completed in September 2014, will perhaps give us more insight into the implications of the severity of this disease for clinical outcome, resource utilisation and finally, quality of life.
of patient characteristics and comorbidities have been highlighted in a few studies (1,9–11). Of note, the observed differences between patient characteristics, comorbidities, and occurrence and outcome of foot ulcer can be dictated by demographics, race and the referral system followed in a particular region or nation (1,9,12–16). Hence, the objective of this study, in keeping with the EURODIALE study (8), was to acquire data on clinical outcome (healing rate, healing time, amputation and death) in newly diagnosed foot ulcer patients with different disease severity and ulcer phenotypes. Presented here are the initial observations from the baseline observation of the enrolled patients.
Department of Burn & Plastic Surgery, Burns Institute, Burn & Plastic Hospital of Chinese PLA General Hospital, Beijing, China 2 Beijing Luhe Hospital, Capital Medical University, Beijing, China 3 Central Hospital of Qilu Petrochemical Hospital Corporation, Shandong, China Correspondence to: Daifeng Hao, Department of Burn & Plastic Surgery, Burns Institute, Burn & Plastic Hospital of PLA General Hospital, No. 51 Fucheng Road, Haidian District, Beijing 100048, China Tel.: +86-10-010-66867972 Fax: +86-10-010-68989181 Email: haodaifeng304@163. com
*These authors contributed equally to this work. Disclosure The authors do not have any conflict of interest, financial or otherwise, to report.
Methods Study design, inclusion and exclusion criteria This study was approved by the Institutional Review Board of the Burn & Plastic Hospital of PLA General Hospital, Beijing, China. One thousand and two consecutive diabetic patients (inclusive of in- and outpatients) presenting with a new foot ulcer between
1161
1162
Contribution of infection and peripheral artery disease
March 2007 and September 2013 were consented to participate in the study. A full-thickness lesion below the ankle was defined as a bona fide foot ulcer (17). Patients who were treated on the same foot for foot ulcer within the last year were excluded from this study. Patients were followed up at intervals of 1 month up to 1 year or complete healing or major amputation, whichever was earlier.
Data collection Data were recorded at onset of participation and during each follow up on standardised case record forms. Focus was made to collect information pertaining to individual (haemoglobin A1c (HbA1c), and serum creatinine levels, comorbidity, previous management and general living conditions) and disease-specific factors that might influence overall management strategies and ultimate outcome. Severe visual impairment (vision 6/24 to 6/60), end-stage renal disease, heart failure and/or angina pectoris (New York Heart Association stage III or IV) and inability to stand or walk without support were classified as disabling comorbidities. The perfusion-extent-depth-infection-sensation system was used to classify the foot ulcers (17,18). An ankle-brachial pressure index (ABPI) of 1.2 and hence not convincing. PAD occurred more frequently in older patients (in 71% of patients aged > 70 years). Disabling comorbidity, other than infection, was present in 79 (severe visual impairment – 33%; end-stage renal disease – 16%; heart failure – 18%; inability to stand or walk – 12%) and 61% (severe visual impairment – 28%;
Table 1 General baseline characteristics of the enrolled patients based on associated peripheral arterial disease (PAD)
Characteristic
Patients with PAD (n = 702)
Age (years) 65 12 Men, n (%) 450 (64.1) Duration of diabetes (%) < 5 years 11.3 5–10 years 13.6 > 10 years 75.1 Deep ulcer (%) 53.2 Size of ulcer (%) < 1 cm2 33.2 1–5 cm2 54.9 > 5 cm2 11.9 Duration of ulcer (%) < 1 week 8.9 1 week–3 months 49.3 > 3 months 41.8 69.3 Glycosylated haemoglobin > 8.4 (%) 79 Disabling comorbidity, other than infection (%) Infection (%) 58.9
Patients without PAD (n = 300)
p-value
58.7 3 197 (65.6)
< 0.001 0.564
12.1 15.3 72.6 48.1
0.487
34.9 52.3 12.8
0.107
9.3 46.5 44.2 53.4
0.149
61
0.038
41.5
< 0.001
0.239
0.006
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
Contribution of infection and peripheral artery disease
end-stage renal disease – 14%; heart failure – 10%; inability to stand or walk – 9%) of diabetic patients with and without PAD, respectively. The percentage of infection in PAD patients (58.9%) was significantly higher than in patients without PAD (41.5%) (p < 0.001). However, there was no difference between the PAD and non-PAD groups in duration of diabetes and depth, severity, or duration of ulcer
Discussion We have presented data on disease severity at presentation and the relationship with patient characteristics in a cross-section of patients with diabetic foot ulcer treated in our hospital between March 2007 and September 2013. Data were obtained in 1002 diabetic patients with a new ulcer and baseline data of enrolled patients are presented here. One of the strengths of this study is that it reflects daily clinical practice. Some of our initial findings are similar to those observed in the now completed EURODIALE study (8), especially that a large per cent of enrolled patients had severe disease with co-occurrence of PAD and infection. However, as opposed to the EURODIALE study, this study did not reveal any significant difference in depth, size and duration of ulcer; of note though our study is still ongoing and the final numbers might see some variation once the final analyses are completed at the conclusion of the study in September 2014. It has been previously shown that the prevalence of PAD varied between 10% and 60% (19–22); however, in this study we saw PAD incidence in 70.05% patients, higher than what had been previously reported. However, it must be noted that the degree of peripheral ischaemia can vary substantially between patients and, unfortunately, physical exami-
References 1 Reiber GE, Vileikyte L, Boyko EJ et al. Causal pathways for incident lower-extremity ulcers in patients with diabetes from two settings. Diabetes Care 1999; 22: 157–62. 2 Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet 2003; 361: 1545–51. 3 Boulton AJ. The diabetic foot: from art to science. The 18th Camillo Golgi lecture. Diabetologia 2004; 47: 1343–53. 4 Reiber GE, Lipsky BA, Gibbons GW. The burden of diabetic foot ulcers. Am J Surg 1998; 176: 5S–10S. 5 Ragnarson Tennvall G, Apelqvist J. Health–economic consequences of diabetic foot lesions. Clin Infect Dis 2004; 39(S2): S132–9. 6 Frykberg RG. An evidence-based approach to diabetic foot infections. Am J Surg 2003; 186: 44S– 54S; discussion 61S–64S. 7 Apelqvist J, Agardh CD. The association between clinical risk factors and outcome of diabetic foot ulcers. Diabetes Res Clin Pract 1992; 18: 43–53. ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
1163
nation is of limited value in resolving such disputes (23). For example, whereas in non-diabetic patients ABPI measurement is an accurate indicator of PAD, in diabetic patients it is not, partly because of noncompressibility of lower limb arteries (23). Indeed, in our study, non-compressible lower leg arteries, with an ABPI of > 1.2 were observed in 43% of the patients. Of note though, as ABPI < 0.9 are indicative of PAD both in non-diabetic and diabetic patients, we are confident that these patients were correctly categorised as having PAD. We also found a relatively high prevalence of infection in patients with PAD (58.9%) as compared with the non-PAD group of patients (41.5%). Our finding of coexistence of infection and PAD corroborates previous findings (9,19,20). It would be interesting to determine at the end of this study whether PAD and infection combination is also associated with the worst outcome among patients, as was observed in the EURODIALE study (8). Our study does have some potential limitations stemming from the fact that is a hospital-based observational study evaluating consecutive patients and diabetic foot ulceration is a recurrent disease (24,25). Furthermore, since patients with an ulcer within the last year were excluded from this study, our patient population is not an exact reflection of the entire population. In conclusion, diabetic foot ulcer is more prominent in patients with PAD that is further reflected by significantly more underlying cases of infection and disabling comorbidity. Followup data on these patients, which will be completed in September 2014, will perhaps give us more insight into the implications of the severity of this disease for clinical outcome, resource utilisation and finally, quality of life.
8 Prompers L, Schaper N, Apelqvist J et al. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study. Diabetologia 2008; 51: 747–55. 9 Armstrong DG, Lavery LA, Harkless LB. Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 1998; 21: 855–9. 10 Ramsey SD, Newton K, Blough D et al. Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999; 22: 382–7. 11 Margolis DJ, Allen-Taylor L, Hoffstad O, Berlin JA. Diabetic neuropathic foot ulcers: the association of wound size, wound duration, and wound grade on healing. Diabetes Care 2002; 25: 1835–9. 12 Mueller MJ, Sinacore DR, Hastings MK, Strube MJ, Johnson JE. Effect of Achilles tendon lengthening on neuropathic plantar ulcers. A randomized clinical trial. J Bone Joint Surg Am 2003; 85-A: 1436–45.
13 Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ. Predictive value of foot pressure assessment as part of a population-based diabetes disease management program. Diabetes Care 2003; 26: 1069–73. 14 Nabuurs-Franssen MH, Sleegers R, Huijberts MS et al. Total contact casting of the diabetic foot in daily practice: a prospective follow up study. Diabetes Care 2005; 28: 243–7. 15 Mueller MJ, Diamond JE, Sinacore DR et al. Total-contact casting in treatment of diabetic plantar ulcers. Controlled clinical trial. Diabetes Care 1989; 12: 384–8. 16 Armstrong DG, Nguyen HC, Lavery LA, van Schie CH, Boulton AJ, Harkless LB. Off-loading the diabetic foot wound: a randomized clinical trial. Diabetes Care 2001; 24: 1019–22. 17 Schaper NC. Diabetic foot ulcer classification system for research purposes: a progress report on criteria for including patients in research studies. Diabetes Metab Res Rev 2004; 20(S1): S90–5.
1164
Contribution of infection and peripheral artery disease
18 Boulton AJ, Gries FA, Jervell JA. Guidelines for the diagnosis and outpatient management of diabetic peripheral neuropathy. Diabet Med 1998; 15: 508– 14. 19 Oyibo SO, Jude EB, Tarawneh I et al. The effects of ulcer size and site, patient’s age, sex and type and duration of diabetes on the outcome of diabetic foot ulcers. Diabet Med 2001; 18: 133–8. 20 Oyibo SO, Jude EB, Tarawneh I, Nguyen HC, Harkless LB, Boulton AJ. A comparison of two diabetic foot ulcer classification systems: the Wagner and the University of Texas wound classification systems. Diabetes Care 2001; 24: 84–8.
21 Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic foot ulcers stratified by etiology. Diabetes Care 2003; 26: 491–4. 22 Apelqvist J, Larsson J, Agardh CD. The importance of peripheral pulses, peripheral oedema and local pain for the outcome of diabetic foot ulcers. Diabet Med 1990; 7: 590–4. 23 Schaper NC, Nabuurs-Franssen MH. The diabetic foot: pathogenesis and clinical evaluation. Semin Vasc Med 2002; 2: 221–8. 24 Lipsky BA, Armstrong DG, Citron DM, Tice AD, Morgenstern DE, Abramson MA. Ertapenem versus piperacillin/tazobactam for diabetic foot infections
(SIDESTEP): prospective, randomised, controlled, double-blinded, multicentre trial. Lancet 2005; 366: 1695–703. 25 Abbott CA, Carrington AL, Ashe H et al.; North-West Diabetes Foot Care Study. The North-West Diabetes Foot Care Study: incidence of, and risk factors for, new diabetic foot ulceration in a community-based patient cohort. Diabet Med 2002; 19: 377–84.
Paper received October 2013, accepted March 2014
ª 2014 John Wiley & Sons Ltd Int J Clin Pract, September 2014, 68, 9, 1161–1164
