DIABETICMedicine DOI: 10.1111/dme.12388
Research: Care Delivery Pre-hospital delay in patients with diabetic foot problems: influencing factors and subsequent quality of care J. Yan, Y. Liu, B. Zhou and M. Sun Department of Endocrinology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China Accepted 12 December 2013
Abstract Aims
To assess pre-hospital patient delay and its associated variables in patients with diabetic foot problems.
Methods We classified 270 patients with diabetic foot problems retrospectively based on the distribution of pre-hospital delay. Clinical, demographic and socio-economic data were collected. Logistic regression analysis was performed to examine independent associations with patient delay. Results The median pre-hospital delay time was 46.49 days. Patients reported short (≤ 1 week; 77 patients, 28.5%), moderate (> 1 week and ≤ 1 month; 106 patients, 39.3%) and long delays (> 1 month; 87 patients, 32.2%). In a univariate analysis, nine variables were associated with a longer delay (P < 0.05): (1) no previous ulcer; (2) no health insurance; (3) poor housing conditions; (4) low income level; (5) low educational level; (6) infrequent foot inspection; (7) few follow-up medical visits; (8) absence of diabetic foot education; (9) lack of knowledge of foot lesion warning signals. A multivariate analysis showed that absence of diabetic foot education (odds ratio 2.70, 95% CI 1.03–7.06, P = 0.043) and lack of knowledge of foot lesion warning signals (odds ratio 2.14, 95% CI 1.16–3.94, P = 0.015) were independent predictors of long patient delay. Long delay increased the risk of amputation (odds ratio 2.22, 95% CI 1.36–3.64, P = 0.002) and mortality (odds ratio 2.69, 95% CI 1.35–5.33, P = 0.005). Conclusions A number of factors were involved in pre-hospital delay among patients with diabetic foot problems and contributed to poor outcomes. We recommend developing a community intervention programme that targets at-risk communities to encourage earlier multidisciplinary team assessment to reduce disparities and improve foot outcomes in patients with diabetes.
Diabet. Med. 31, 624–629 (2014)
Introduction Diabetic foot problems, a serious complication of diabetes, rapidly progress and can result in disability, high mortality and costly expenses in China and throughout the world [1,2]. Despite recent advances in identifying effective treatments for diabetic foot problems [3,4], there are substantial difficulties in implementing these therapies, particularly in resource-poor areas, such as Chongqing, China. A weak but critical link in the chain of events leading to prompt and effective treatment is patient delay in seeking medical care. Limited evidence has demonstrated that recognizing diabetic Correspondence to: Bo Zhou. E-mail: [email protected]
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foot problems early, combined with the early involvement of a multidisciplinary foot care team, may significantly improve patient outcomes [5–7]. However, pre-hospital delay remain unacceptably long, with median intervals that average 26–92 days [6,8,9]. Interventions to reduce delay have met with limited success [10,11]. A better understanding of the factors contributing to diabetic foot problems will stimulate new approaches to reduce pre-hospital delay. In this study, we aim to investigate the factors that contribute to patient delay in reporting diabetic foot problems, compare its consequent outcomes and analyse the reasons for the pre-hospital delay. Thus far, little research has been conducted on patients with diabetes with respect to delay in reporting new foot problems.
ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
Research article
What’s new? • This study represents the first examination of pre-hospital delay in patients with diabetic foot problems in China. • A number of factors were involved in patient delay and contributed to their poor outcomes.
Patients and methods Study design
This cross-sectional, retrospective, single-centre survey was conducted in the first teaching hospital of Chongqing Medical University, a tertiary care setting, between May 2007 and May 2012. A patient with diabetic foot problems must have experienced at least one of the following inclusion criteria: (1) an ulcer, blister or break in the skin of the foot; (2) inflammation or swelling on any part of the foot, or any sign of infection; (3) unexplained foot pain; (4) fracture or dislocation in the foot, with no prior history of significant trauma; or (5) gangrene of all or part of the foot. The following exclusion criteria were applied: (1) diabetic foot problems were not the dominant clinical factor for inpatient care; (2) the patients had communication problems (serious hearing or cognitive impairment); or (3) the patients refused to participate in the investigation. The time interval of the pre-hospital delay was defined as the time elapsed between the onset of symptoms and hospital admission. Based on the distribution of delay intervals in this study sample, the cut-off points of ≤ 1 week, ≤ 1 month and > 1 month were chosen to distinguish between short, moderate and long delays after symptom onset of diabetic foot problems. Data and definitions
We collected data by reviewing the patients’ medical records and through structured interviews. Taking into consideration that some patients had two or more medical records because of recurrent ulcers and that we aimed to avoid double counting patients, we performed the following steps: for patients with lower-extremity amputation as a result of diabetic foot problems, we analysed the data from the hospitalization relating to the amputation closest to the proximal end of any limbs; and for patients with diabetic foot problems without lower-extremity amputation, we analysed the data at the time of the latest admission. We obtained the following data from the hospital admissions: (1) demographics, such as age, gender, BMI, smoking habits, alcohol intake and health insurance coverage; (2) information related to diabetes (i.e. type of diabetes, duration of diabetes and treatment measures); (3) laboratory tests, including haemoglobin, HbA1c, white blood cells, serum albumin, serum creatinine and lipid profile; (4) information
ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
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related to diabetic foot problems, such as the history of previous ulcers, antecedent contributory factors, Wagner grade [12], antibiotic choices, debridement disposal and revascularization; (5) other diabetic complications, such as diabetic neuropathy, a spot urinary microalbumin/creatine ratio, estimated glomerular filtration rate (eGFR), ankle– brachial pressure index and visual change; (6) other co-morbidities, such as cardiovascular disease, cerebrovascular disease and hypertension, which were diagnosed by the treating physicians and documented in the medical records; and (7) observed outcomes, such as hospital stays and amputation and mortality rates. Diabetic peripheral neuropathy was diagnosed when two or more of the following criteria were present: symptoms, sensory signs, motor signs and nerve conduction abnormalities [13,14]. Estimated GFR was calculated according to the Modification of Diet in Renal Disease formula. Visual change was categorized as good or bad; that is, visual acuity above 20/40 was classified as good and visual acuity below 20/40 was classified as bad. Amputation included major and minor amputations. Mortality was defined as death caused by ischaemic heart disease, acute pulmonary oedema, acute congestive heart failure, cardiogenic shock, stroke, sudden death, pulmonary embolism or sepsis [2]. Structured interviews were conducted to obtain information about the following: (1) housing conditions, which were classified based on our local average per capita living space (good corresponded to a mean housing area of ≥ 40 m2, bad was < 20 m2 and moderate was ≥ 20 m2 and < 40 m2; (2) education level, which was coded as primary school (≤ 6 years), secondary school (6–12 years) and university or college (> 12 years); (3) income level, which was classified by salary [≥ 4000 renminbi (RMB) yuan per month was high, < 2000 RMB yuan per month was low, and salaries between both grades were moderate]; (4) cohabitation status (living with others or living alone); (5) the patient’s foot inspection routine (a frequency of foot inspection ≥ 5 times per week was ‘usually’, between two and five times per week was ‘sometimes’ and less than twice per week was ‘seldom’); (6) wearing suitable shoes and walking barefoot; (7) frequency of visits to the diabetic clinic; and (8) knowledge of the danger signs of foot lesions and relevant diabetic foot education. The contents of the material regarding diabetic foot education were based on the International Consensus and Practical Guidelines on the Management and the Prevention of the Diabetic Foot (http://www.ncbi.nlm.nih. gov/pubmed/14611743).
Statistical analysis
A descriptive analysis was conducted to assess the characteristics of the samples. Categorical data are expressed as numbers and the v2-test or Fisher’s exact test was used to evaluate the distribution differences. The normally distributed continuous variables are expressed as the mean standard deviation (SD). Non-normally distributed variables are
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expressed as the median with interquartile range and logarithmic transformation was used to make them normal. The differences were tested with the F-test. A multivariable logistic regression analysis was performed to assess which characteristics and clinical variables were independently associated with pre-hospital delay using variables with P < 0.05, according to the univariate analysis. Another logistic regression analysis was performed to assess the association between the pre-hospital delay time and poor outcomes (amputation and mortality). We conducted all analyses using SPSS version 17.0 statistical software (SPSS Inc., Chicago, IL, USA); P < 0.05 was considered statistically significant.
Results Characteristics of the study population
During the study period, 270 patients (mean age 65.71 years) were eligible for analysis. Of these patients, 158 (58.5%) were men and six (2.2%) had Type 1 diabetes. Of the patients, approximately 25.6% were smokers and 23.7% were alcohol drinkers, all of whom were men. A total of 77 (28.5%) patients arrived at the hospital within 1 week of symptom onset, 106 (39.3%) patients arrived between 1 week and 1 month after symptom onset and the remaining patients were
Table 1 Comparison of the characteristics of the three groups All (n = 270) Demographics Gender (male/female) Age (years) BMI (kg/m2) Smoking habit (yes/no) Alcohol misuse (yes/no) Diabetic history Type of diabetes (Type 2/Type 1) Diabetic duration (years) Diabetes treatment: no treatment/oral drugs/insulin Laboratory test HbA1c (mmol/mol) HbA1c (%) Haemoglobin (g/l)
158/112 65.71 11.73 22.57 3.16 69/201 64/206
45/32 63.75 12.52 22.97 2.90 23/54 20/57
264/6
75/2
103/3
P†
P‡
50/37 68.01 11.34 21.83 2.98 25/62 19/68
0.963 0.059 0.068 0.217 0.824
— — — — —
86/1
0.708
—
8.43 5.74 11/50/45
9.90 7.63 11/31/45
0.051 0.392
— —
78 32 9.25 2.92 112.79 21.16
74 32 8.93 2.93 118.76 18.02
83 33 9.70 3.00 113.47 20.92
75 30 9.00 2.78 106.47 22.57
0.214 0.214 0.001
6.91 (5.42–10.02) 35.54 5.20 79.00 (61.00–107.75) 4.02 1.16 2.18 0.89 1.19 (0.92–1.74) 1.07 0.37
7.30 (5.87–9.49) 34.10 6.39 76.00 (55.00–112.00) 4.06 1.27 2.27 0.99 1.13 (0.85–1.89) 1.01 0.39
7.12 (5.80–10.25) 33.71 5.92 80.00 (61.00–113.00) 4.34 1.33 2.44 1.02 1.20 (0.88–1.63) 1.14 0.39
0.778
— — 1 vs. 3§, 2 vs. 3¶ —
0.121 0.690
— —
0.280 0.311 0.836
— — —
0.144
—
Serum albumin (g/l) Serum creatinine (lmol/l)*
34.39 5.93 79.00 (59.75–112.00) 4.13 1.25 2.29 0.97 1.16 (0.88–1.73)
Debridement (yes/no) Antibiotics (≤ 1/≥ 2)
63/43 65.25 11.24 22.84 3.41 21/85 25/81
Group 3 (n = 87)
11.12 8.94 5/35/37
7.12 (5.65–9.89)
HDL (mmol/l) Diabetic foot information Antecedent factors (yes/no) Wagner grade (< 4/≥ 4)
Group 2 (n = 106)
9.67 7.44 27/116/127
White blood cells (103/ll)*
Total cholesterol (mmol/l) LDL cholesterol (mmol/l) Triglycerides (mmol/l)*
Group 1 (n = 77)
1.07 0.39
— 1 vs. 3§, 2 vs. 3§ — 1 vs. 2§, 1 vs. 3§
86/184 208/62
23/54 67/10
37/69 90/16
26/61 51/36
0.687 < 0.001
104/166 135/135
30/47 51/26
40/66 44/62
34/53 40/47
0.978 0.003
2/75
4/102
9/78
0.057
—
0.568
—
0.505 0.479 0.325 0.150 0.871 0.403 0.855
— — — — — — —
Revascularization (yes/no) 15/255 Other complications and co-morbidities Urinary microalbumin/creatine 47.00 ratio (mg/g.Cr)* (16.60–168.05) eGFR (ml min 1 1.73 m 2) 85.50 40.06 Ankle–brachial pressure index 0.95 0.28 Diabetic neuropathy (yes/no) 223/47 Visual acuity (good/bad) 112/158 Hypertension (yes/no) 147/123 Cardiac heart disease (yes/no) 39/231 History of stroke (yes/no) 25/245
36.10 (15.90–103.20) 86.30 37.33 0.92 0.30 67/10 39/38 40/37 12/65 7/70
51.10 (28.30–164.40) 88.60 42.68 0.94 0.23 88/18 41/65 59/47 18/88 11/95
60.40 (13.90–262.30) 80.83 39.46 1.01 0.31 68/19 32/55 48/39 9/78 7/80
eGFR, estimated glomerular filtration rate. Group 1, short-delay patients; group 2, moderate-delay patients; group 3, long-delay patients. *Non-normal distribution; †overall differences between groups; ‡significant difference from groups (§P < 0.01; ¶P < 0.05).
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admitted to the hospital 1 month after the onset of symptoms. Although most characteristics had no significant differences between the delayed groups, the patients with long pre-hospital delay were more likely to have lower haemoglobin, have Wagner grade ≥ 4 [12] and use at least two types of antibiotics compared with those patients with short pre-hospital delay (Table 1).
In a multivariate logistic regression analysis, the absence of diabetic foot education (odds ratio 2.70, 95% CI 1.03–7.06, P = 0.043) and the lack of knowledge of foot lesion danger signals (odds ratio 2.14, 95% CI 1.16–3.94, P = 0.015) were independently associated with a long pre-hospital delay time, indicating that those patients who had received diabetic foot education and had diabetic foot problems knowledge would seek early and immediate medical care (Table 3).
Pre-hospital delay and consequent outcomes
Patients with long pre-hospital delay were more likely to undergo an amputation (odds ratio 2.22, 95% CI 1.36–3.64, P = 0.002) and die (odds ratio 2.69, 95% CI 1.35–5.33, P = 0.005) than those with short pre-hospital delay. Although patients with long pre-hospital delay had longer hospital stays, there was no significant difference (Table 2).
Pre-hospital delay and associated variables
The median pre-hospital delay time was 46.49 days. Patients with short pre-hospital delay more often had histories of foot ulcer, medical insurance coverage, good housing conditions and high income. Additionally, patients with long pre-hospital delay were less likely to have accomplished the following tasks compared with patients with short pre-hospital delay: inspect their feet frequently, follow-up regularly with physicians, receive foot education and know about foot lesion danger signals.
Discussion Pre-hospital delay in patients with acute coronary syndrome has been described in previous studies [15,16]; however, this systematic study is among the first to examine pre-hospital delays in patients with diabetic foot problems, which describes the time elapsed from detecting diabetic foot problems to seeking medical care in a hospital that implements a multidisciplinary approach to diabetic foot problem management. Although this elapsed time may underestimate the exact delay time because the usual risk factors, including diabetic neuropathy and poor vision, can cause inattention and lead to a delay in detecting foot problems, only 12 (4.4%) patients of our study reported their foot problems within 24 h. The median pre-hospital delay time was 46.49 days. More importantly, our study demonstrates that a long pre-hospital delay can increase risks of lowerextremity amputation and mortality. Furthermore, a history of foot ulcer, good socio-economic status, adequate self-care
Table 2 Comparison of the observed outcomes and previous ulcers, socio-economic status, foot care and behavioural characteristics of the three groups
Hospital stay (days)* Amputation (yes/no) Mortality (yes/no) Previous ulcers (yes/no) Medical insurance (yes/no) Housing conditions (good/moderate/bad) Income level (high/moderate/low) Educational level (primary school/secondary school/university) Live alone (yes/no) Wearing suitable shoes (yes/no) Walking barefoot (occasionally/never) Performance of foot inspection (usually/sometimes/seldom) Diabetic clinic visits (> 2/1–2/< 1 per year) Foot education received (yes/no) Knowledge of foot lesion danger signals (yes/no)
P†
P‡
All
Group 1
Group 2
Group 3
14.00 (8.00–26.00) 38/232 21/249 86/184 184/86 85/138/7
13.00 (8.00–20.00) 5/72 2/75 39/38 65/12 39/28/0
14.00 (8.00–27.25) 12/94 6/100 21/85 69/37 26/58/3
17.00 (9.00–28.00) 21/66 13/74 26/a 50/37 20/52/4
0.003 0.008 < 0.001 0.001 < 0.001
1 vs. 3§, 2 vs. 3¶ 1 vs. 3§, 2 vs. 3¶ 1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§
37/26/4
22/42/23
17/41/18
< 0.001
1 vs. 2§, 1 vs. 3§
32/45/10
23/47/6
0.002
1 vs. 2§, 1 vs. 3§
76/109/45 63/135/32
8/43/16
0.494
—
17/213 209/21
4/63 64/3
7/80 78/9
6/70 67/9
0.869 0.276
— —
27/203
3/64
11/76
13/63
0.061
—
70/132/28
32/32/3
26/51/10
12/49/15
< 0.001
1 vs. 2¶, 1 vs. 3§
65/143/22
28/37/2
22/56/9
15/50/11
0.015
1 vs. 2¶, 1 vs. 3§
67/0 43/24
77/10 30/57
60/16 18/58
< 0.001 < 0.001
1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§
204/26 91/139
*Non-normal distribution; †overall differences between groups; ‡significant difference from groups (§P < 0.01; ¶P < 0.05).
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Table 3 Regression analysis assessing the associations between pre-hospital delay and risk factors
Odds ratio
95% CI of odds ratio
Previous ulcers No 1.45 0.84–2.53 Yes Reference Medical insurance No 1.07 0.55–2.09 Yes Reference Housing conditions Bad 1.74 0.23–13.28 Moderate 0.59 0.18–1.87 Good Reference Income level Low 1.70 0.41–7.03 Moderate 2.41 0.79–7.39 High Reference Educational level Primary school 1.19 0.43–3.26 Secondary school 1.13 0.48–2.69 University Reference Performance of foot inspection Seldom 2.27 0.81–6.37 Sometimes 1.78 0.93–3.42 Usually Reference Diabetic clinic visits < 1 per year 1.35 0.42–4.26 1–2 per year 1.11 0.57–2.17 > 2 per year Reference Foot education received No 2.70 1.03–7.06 Yes Reference Knowledge of foot lesion danger signals No 2.14 1.16–3.94 Yes Reference
P
0.182
0.836
0.595 0.366
0.461 0.124
0.738 0.774
0.121 0.082
0.613 0.756
0.043
0.015
behaviours and more diabetic foot problem knowledge were associated with a short pre-hospital delay. The UK National Institute for Health and Clinical Excellence (NICE) (now known as the National Institute for Health and Care Excellence) recommends referral of patients with diabetic foot problems to a multidisciplinary foot care team within 24 h of the initial examination of the patient’s feet [17]. However, the availability of this strategy was limited because the majority (71.5%) of patients were admitted to the hospital 1 week after symptom onset in our study. Additionally, our findings suggest that a long pre-hospital delay is a major contributor to the morbidity of patients with diabetic foot problems, because a significant number of individuals who delay seeking care develop potentially preventable complications. This finding agrees with two other studies [9,18], which observed that a long pre-hospital delay contributed to deteriorating diabetic foot problems and resulted in amputation and mortality. Mild diabetic foot problems can progress to severe limb-threatening infection, sepsis and gangrene when these conditions are untreated, thereby putting the patients at increased risk for wound-related amputation and death [9]. Additionally, persistent inflammation and long-term fluctuating blood sugar levels can trigger cardiovascular events and increase
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the potential for death caused by ischaemic heart disease [19]. Patients with a history of myocardial infarction or stroke generally have a shorter pre-hospital delay among patients with acute coronary syndrome [20,21]. We found a similar result: patients with a history of foot ulcers also had a shorter pre-hospital delay than those without these events. Because pre-hospital delay reflects the patient’s own decision-making process, a previous ulcer or limb-threatening event might have led to greater symptom awareness, efficient evaluation and quicker decision making. However, Mantey et al. [22] did not detect any such relationship, possibly because of a different definition of ‘delay’ or a different study design. The decision to seek treatment is heavily influenced by the patient’s social context, cognitive process and economic situation, but these delay factors have not been fully explored. Lower socio-economic status prolongs pre-hospital delay time in patients with acute coronary syndrome [21,23]. Our findings show that lack of medical insurance, poor housing conditions, low income and low educational level were associated with a long pre-hospital delay in patients with diabetic foot problems. Although few researchers have studied the association between socio-economic status and pre-hospital delay time in patients with diabetic foot problems, Weng et al. [24] demonstrated that low socio-economic status was linked to increased morbidity and premature mortality in people with diabetes. One possible explanation is that patients with low socio-economic status do not seek medical care because they lack access, either physically or financially, to health care; another explanation is that patients with a low level of education lack vital knowledge and sensitivity about their illness and its consequences. Patients who receive education and training in the diabetic foot care programme have learned to seek immediate medical assistance when they find lesions on their feet [25]. In this study, diabetic foot education and knowledge of foot lesion danger signals were independently associated with pre-hospital delay. We stress the importance of providing education and information on self-care behaviours in diabetic foot problems. Patients with diabetic foot problem knowledge often have sufficient information about the recognition, causes, symptoms, management and consequences of diabetic foot problems. Therefore, patients with diabetic foot problem knowledge are fully prepared to self-manage tasks, such as following up regularly, inspecting their feet frequently, detecting foot problems promptly, and seeking early and immediate medical care.
Conclusions There are significant and potentially modifiable factors for pre-hospital delay in patients with diabetic foot problems. These delays are most marked in patients who have no previous history of foot problems, no medical insurance, poor housing conditions, low income, low levels of
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Research article
education, infrequent foot inspections, few follow-up medical visits, no diabetic foot education and lack of knowledge of foot lesion danger signals. A long pre-hospital delay is likely to contribute significantly to these poorer outcomes, lower-extremity amputation and mortality. We recommend developing a community intervention programme targeting at-risk communities to encourage earlier assessment by a multidisciplinary team to reduce disparity and improve foot outcomes in patients with diabetes.
Limitations
First, this study used arbitrary cut-off scores based on the 33rd and 66th percentiles to differentiate between short and long pre-hospital delays. However, there is no standard criterion on short or long pre-hospital delay times in the literature. Second, the data set used in this study was generated from one hospital, limiting its generalizability to other hospitals; therefore, additional large-scale research is needed. Third, the exclusion criteria may have introduced a bias because the patients who had communication problems and refused to participate in the study often demonstrated poor compliance, which may have caused delays in the detection of their foot problems and led to their delayed admission. Finally, retrospective surveys have inherent deficiencies. A prospective design would be preferable to establish the direction of causality.
Funding
This study was funded by the National Key Clinical Department Construction Project.
Competing interests
None declared.
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Research: Care Delivery Pre-hospital delay in patients with diabetic foot problems: influencing factors and subsequent quality of care J. Yan, Y. Liu, B. Zhou and M. Sun Department of Endocrinology, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China Accepted 12 December 2013
Abstract Aims
To assess pre-hospital patient delay and its associated variables in patients with diabetic foot problems.
Methods We classified 270 patients with diabetic foot problems retrospectively based on the distribution of pre-hospital delay. Clinical, demographic and socio-economic data were collected. Logistic regression analysis was performed to examine independent associations with patient delay. Results The median pre-hospital delay time was 46.49 days. Patients reported short (≤ 1 week; 77 patients, 28.5%), moderate (> 1 week and ≤ 1 month; 106 patients, 39.3%) and long delays (> 1 month; 87 patients, 32.2%). In a univariate analysis, nine variables were associated with a longer delay (P < 0.05): (1) no previous ulcer; (2) no health insurance; (3) poor housing conditions; (4) low income level; (5) low educational level; (6) infrequent foot inspection; (7) few follow-up medical visits; (8) absence of diabetic foot education; (9) lack of knowledge of foot lesion warning signals. A multivariate analysis showed that absence of diabetic foot education (odds ratio 2.70, 95% CI 1.03–7.06, P = 0.043) and lack of knowledge of foot lesion warning signals (odds ratio 2.14, 95% CI 1.16–3.94, P = 0.015) were independent predictors of long patient delay. Long delay increased the risk of amputation (odds ratio 2.22, 95% CI 1.36–3.64, P = 0.002) and mortality (odds ratio 2.69, 95% CI 1.35–5.33, P = 0.005). Conclusions A number of factors were involved in pre-hospital delay among patients with diabetic foot problems and contributed to poor outcomes. We recommend developing a community intervention programme that targets at-risk communities to encourage earlier multidisciplinary team assessment to reduce disparities and improve foot outcomes in patients with diabetes.
Diabet. Med. 31, 624–629 (2014)
Introduction Diabetic foot problems, a serious complication of diabetes, rapidly progress and can result in disability, high mortality and costly expenses in China and throughout the world [1,2]. Despite recent advances in identifying effective treatments for diabetic foot problems [3,4], there are substantial difficulties in implementing these therapies, particularly in resource-poor areas, such as Chongqing, China. A weak but critical link in the chain of events leading to prompt and effective treatment is patient delay in seeking medical care. Limited evidence has demonstrated that recognizing diabetic Correspondence to: Bo Zhou. E-mail: [email protected]
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foot problems early, combined with the early involvement of a multidisciplinary foot care team, may significantly improve patient outcomes [5–7]. However, pre-hospital delay remain unacceptably long, with median intervals that average 26–92 days [6,8,9]. Interventions to reduce delay have met with limited success [10,11]. A better understanding of the factors contributing to diabetic foot problems will stimulate new approaches to reduce pre-hospital delay. In this study, we aim to investigate the factors that contribute to patient delay in reporting diabetic foot problems, compare its consequent outcomes and analyse the reasons for the pre-hospital delay. Thus far, little research has been conducted on patients with diabetes with respect to delay in reporting new foot problems.
ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
Research article
What’s new? • This study represents the first examination of pre-hospital delay in patients with diabetic foot problems in China. • A number of factors were involved in patient delay and contributed to their poor outcomes.
Patients and methods Study design
This cross-sectional, retrospective, single-centre survey was conducted in the first teaching hospital of Chongqing Medical University, a tertiary care setting, between May 2007 and May 2012. A patient with diabetic foot problems must have experienced at least one of the following inclusion criteria: (1) an ulcer, blister or break in the skin of the foot; (2) inflammation or swelling on any part of the foot, or any sign of infection; (3) unexplained foot pain; (4) fracture or dislocation in the foot, with no prior history of significant trauma; or (5) gangrene of all or part of the foot. The following exclusion criteria were applied: (1) diabetic foot problems were not the dominant clinical factor for inpatient care; (2) the patients had communication problems (serious hearing or cognitive impairment); or (3) the patients refused to participate in the investigation. The time interval of the pre-hospital delay was defined as the time elapsed between the onset of symptoms and hospital admission. Based on the distribution of delay intervals in this study sample, the cut-off points of ≤ 1 week, ≤ 1 month and > 1 month were chosen to distinguish between short, moderate and long delays after symptom onset of diabetic foot problems. Data and definitions
We collected data by reviewing the patients’ medical records and through structured interviews. Taking into consideration that some patients had two or more medical records because of recurrent ulcers and that we aimed to avoid double counting patients, we performed the following steps: for patients with lower-extremity amputation as a result of diabetic foot problems, we analysed the data from the hospitalization relating to the amputation closest to the proximal end of any limbs; and for patients with diabetic foot problems without lower-extremity amputation, we analysed the data at the time of the latest admission. We obtained the following data from the hospital admissions: (1) demographics, such as age, gender, BMI, smoking habits, alcohol intake and health insurance coverage; (2) information related to diabetes (i.e. type of diabetes, duration of diabetes and treatment measures); (3) laboratory tests, including haemoglobin, HbA1c, white blood cells, serum albumin, serum creatinine and lipid profile; (4) information
ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
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related to diabetic foot problems, such as the history of previous ulcers, antecedent contributory factors, Wagner grade [12], antibiotic choices, debridement disposal and revascularization; (5) other diabetic complications, such as diabetic neuropathy, a spot urinary microalbumin/creatine ratio, estimated glomerular filtration rate (eGFR), ankle– brachial pressure index and visual change; (6) other co-morbidities, such as cardiovascular disease, cerebrovascular disease and hypertension, which were diagnosed by the treating physicians and documented in the medical records; and (7) observed outcomes, such as hospital stays and amputation and mortality rates. Diabetic peripheral neuropathy was diagnosed when two or more of the following criteria were present: symptoms, sensory signs, motor signs and nerve conduction abnormalities [13,14]. Estimated GFR was calculated according to the Modification of Diet in Renal Disease formula. Visual change was categorized as good or bad; that is, visual acuity above 20/40 was classified as good and visual acuity below 20/40 was classified as bad. Amputation included major and minor amputations. Mortality was defined as death caused by ischaemic heart disease, acute pulmonary oedema, acute congestive heart failure, cardiogenic shock, stroke, sudden death, pulmonary embolism or sepsis [2]. Structured interviews were conducted to obtain information about the following: (1) housing conditions, which were classified based on our local average per capita living space (good corresponded to a mean housing area of ≥ 40 m2, bad was < 20 m2 and moderate was ≥ 20 m2 and < 40 m2; (2) education level, which was coded as primary school (≤ 6 years), secondary school (6–12 years) and university or college (> 12 years); (3) income level, which was classified by salary [≥ 4000 renminbi (RMB) yuan per month was high, < 2000 RMB yuan per month was low, and salaries between both grades were moderate]; (4) cohabitation status (living with others or living alone); (5) the patient’s foot inspection routine (a frequency of foot inspection ≥ 5 times per week was ‘usually’, between two and five times per week was ‘sometimes’ and less than twice per week was ‘seldom’); (6) wearing suitable shoes and walking barefoot; (7) frequency of visits to the diabetic clinic; and (8) knowledge of the danger signs of foot lesions and relevant diabetic foot education. The contents of the material regarding diabetic foot education were based on the International Consensus and Practical Guidelines on the Management and the Prevention of the Diabetic Foot (http://www.ncbi.nlm.nih. gov/pubmed/14611743).
Statistical analysis
A descriptive analysis was conducted to assess the characteristics of the samples. Categorical data are expressed as numbers and the v2-test or Fisher’s exact test was used to evaluate the distribution differences. The normally distributed continuous variables are expressed as the mean standard deviation (SD). Non-normally distributed variables are
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expressed as the median with interquartile range and logarithmic transformation was used to make them normal. The differences were tested with the F-test. A multivariable logistic regression analysis was performed to assess which characteristics and clinical variables were independently associated with pre-hospital delay using variables with P < 0.05, according to the univariate analysis. Another logistic regression analysis was performed to assess the association between the pre-hospital delay time and poor outcomes (amputation and mortality). We conducted all analyses using SPSS version 17.0 statistical software (SPSS Inc., Chicago, IL, USA); P < 0.05 was considered statistically significant.
Results Characteristics of the study population
During the study period, 270 patients (mean age 65.71 years) were eligible for analysis. Of these patients, 158 (58.5%) were men and six (2.2%) had Type 1 diabetes. Of the patients, approximately 25.6% were smokers and 23.7% were alcohol drinkers, all of whom were men. A total of 77 (28.5%) patients arrived at the hospital within 1 week of symptom onset, 106 (39.3%) patients arrived between 1 week and 1 month after symptom onset and the remaining patients were
Table 1 Comparison of the characteristics of the three groups All (n = 270) Demographics Gender (male/female) Age (years) BMI (kg/m2) Smoking habit (yes/no) Alcohol misuse (yes/no) Diabetic history Type of diabetes (Type 2/Type 1) Diabetic duration (years) Diabetes treatment: no treatment/oral drugs/insulin Laboratory test HbA1c (mmol/mol) HbA1c (%) Haemoglobin (g/l)
158/112 65.71 11.73 22.57 3.16 69/201 64/206
45/32 63.75 12.52 22.97 2.90 23/54 20/57
264/6
75/2
103/3
P†
P‡
50/37 68.01 11.34 21.83 2.98 25/62 19/68
0.963 0.059 0.068 0.217 0.824
— — — — —
86/1
0.708
—
8.43 5.74 11/50/45
9.90 7.63 11/31/45
0.051 0.392
— —
78 32 9.25 2.92 112.79 21.16
74 32 8.93 2.93 118.76 18.02
83 33 9.70 3.00 113.47 20.92
75 30 9.00 2.78 106.47 22.57
0.214 0.214 0.001
6.91 (5.42–10.02) 35.54 5.20 79.00 (61.00–107.75) 4.02 1.16 2.18 0.89 1.19 (0.92–1.74) 1.07 0.37
7.30 (5.87–9.49) 34.10 6.39 76.00 (55.00–112.00) 4.06 1.27 2.27 0.99 1.13 (0.85–1.89) 1.01 0.39
7.12 (5.80–10.25) 33.71 5.92 80.00 (61.00–113.00) 4.34 1.33 2.44 1.02 1.20 (0.88–1.63) 1.14 0.39
0.778
— — 1 vs. 3§, 2 vs. 3¶ —
0.121 0.690
— —
0.280 0.311 0.836
— — —
0.144
—
Serum albumin (g/l) Serum creatinine (lmol/l)*
34.39 5.93 79.00 (59.75–112.00) 4.13 1.25 2.29 0.97 1.16 (0.88–1.73)
Debridement (yes/no) Antibiotics (≤ 1/≥ 2)
63/43 65.25 11.24 22.84 3.41 21/85 25/81
Group 3 (n = 87)
11.12 8.94 5/35/37
7.12 (5.65–9.89)
HDL (mmol/l) Diabetic foot information Antecedent factors (yes/no) Wagner grade (< 4/≥ 4)
Group 2 (n = 106)
9.67 7.44 27/116/127
White blood cells (103/ll)*
Total cholesterol (mmol/l) LDL cholesterol (mmol/l) Triglycerides (mmol/l)*
Group 1 (n = 77)
1.07 0.39
— 1 vs. 3§, 2 vs. 3§ — 1 vs. 2§, 1 vs. 3§
86/184 208/62
23/54 67/10
37/69 90/16
26/61 51/36
0.687 < 0.001
104/166 135/135
30/47 51/26
40/66 44/62
34/53 40/47
0.978 0.003
2/75
4/102
9/78
0.057
—
0.568
—
0.505 0.479 0.325 0.150 0.871 0.403 0.855
— — — — — — —
Revascularization (yes/no) 15/255 Other complications and co-morbidities Urinary microalbumin/creatine 47.00 ratio (mg/g.Cr)* (16.60–168.05) eGFR (ml min 1 1.73 m 2) 85.50 40.06 Ankle–brachial pressure index 0.95 0.28 Diabetic neuropathy (yes/no) 223/47 Visual acuity (good/bad) 112/158 Hypertension (yes/no) 147/123 Cardiac heart disease (yes/no) 39/231 History of stroke (yes/no) 25/245
36.10 (15.90–103.20) 86.30 37.33 0.92 0.30 67/10 39/38 40/37 12/65 7/70
51.10 (28.30–164.40) 88.60 42.68 0.94 0.23 88/18 41/65 59/47 18/88 11/95
60.40 (13.90–262.30) 80.83 39.46 1.01 0.31 68/19 32/55 48/39 9/78 7/80
eGFR, estimated glomerular filtration rate. Group 1, short-delay patients; group 2, moderate-delay patients; group 3, long-delay patients. *Non-normal distribution; †overall differences between groups; ‡significant difference from groups (§P < 0.01; ¶P < 0.05).
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ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
Research article
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admitted to the hospital 1 month after the onset of symptoms. Although most characteristics had no significant differences between the delayed groups, the patients with long pre-hospital delay were more likely to have lower haemoglobin, have Wagner grade ≥ 4 [12] and use at least two types of antibiotics compared with those patients with short pre-hospital delay (Table 1).
In a multivariate logistic regression analysis, the absence of diabetic foot education (odds ratio 2.70, 95% CI 1.03–7.06, P = 0.043) and the lack of knowledge of foot lesion danger signals (odds ratio 2.14, 95% CI 1.16–3.94, P = 0.015) were independently associated with a long pre-hospital delay time, indicating that those patients who had received diabetic foot education and had diabetic foot problems knowledge would seek early and immediate medical care (Table 3).
Pre-hospital delay and consequent outcomes
Patients with long pre-hospital delay were more likely to undergo an amputation (odds ratio 2.22, 95% CI 1.36–3.64, P = 0.002) and die (odds ratio 2.69, 95% CI 1.35–5.33, P = 0.005) than those with short pre-hospital delay. Although patients with long pre-hospital delay had longer hospital stays, there was no significant difference (Table 2).
Pre-hospital delay and associated variables
The median pre-hospital delay time was 46.49 days. Patients with short pre-hospital delay more often had histories of foot ulcer, medical insurance coverage, good housing conditions and high income. Additionally, patients with long pre-hospital delay were less likely to have accomplished the following tasks compared with patients with short pre-hospital delay: inspect their feet frequently, follow-up regularly with physicians, receive foot education and know about foot lesion danger signals.
Discussion Pre-hospital delay in patients with acute coronary syndrome has been described in previous studies [15,16]; however, this systematic study is among the first to examine pre-hospital delays in patients with diabetic foot problems, which describes the time elapsed from detecting diabetic foot problems to seeking medical care in a hospital that implements a multidisciplinary approach to diabetic foot problem management. Although this elapsed time may underestimate the exact delay time because the usual risk factors, including diabetic neuropathy and poor vision, can cause inattention and lead to a delay in detecting foot problems, only 12 (4.4%) patients of our study reported their foot problems within 24 h. The median pre-hospital delay time was 46.49 days. More importantly, our study demonstrates that a long pre-hospital delay can increase risks of lowerextremity amputation and mortality. Furthermore, a history of foot ulcer, good socio-economic status, adequate self-care
Table 2 Comparison of the observed outcomes and previous ulcers, socio-economic status, foot care and behavioural characteristics of the three groups
Hospital stay (days)* Amputation (yes/no) Mortality (yes/no) Previous ulcers (yes/no) Medical insurance (yes/no) Housing conditions (good/moderate/bad) Income level (high/moderate/low) Educational level (primary school/secondary school/university) Live alone (yes/no) Wearing suitable shoes (yes/no) Walking barefoot (occasionally/never) Performance of foot inspection (usually/sometimes/seldom) Diabetic clinic visits (> 2/1–2/< 1 per year) Foot education received (yes/no) Knowledge of foot lesion danger signals (yes/no)
P†
P‡
All
Group 1
Group 2
Group 3
14.00 (8.00–26.00) 38/232 21/249 86/184 184/86 85/138/7
13.00 (8.00–20.00) 5/72 2/75 39/38 65/12 39/28/0
14.00 (8.00–27.25) 12/94 6/100 21/85 69/37 26/58/3
17.00 (9.00–28.00) 21/66 13/74 26/a 50/37 20/52/4
0.003 0.008 < 0.001 0.001 < 0.001
1 vs. 3§, 2 vs. 3¶ 1 vs. 3§, 2 vs. 3¶ 1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§
37/26/4
22/42/23
17/41/18
< 0.001
1 vs. 2§, 1 vs. 3§
32/45/10
23/47/6
0.002
1 vs. 2§, 1 vs. 3§
76/109/45 63/135/32
8/43/16
0.494
—
17/213 209/21
4/63 64/3
7/80 78/9
6/70 67/9
0.869 0.276
— —
27/203
3/64
11/76
13/63
0.061
—
70/132/28
32/32/3
26/51/10
12/49/15
< 0.001
1 vs. 2¶, 1 vs. 3§
65/143/22
28/37/2
22/56/9
15/50/11
0.015
1 vs. 2¶, 1 vs. 3§
67/0 43/24
77/10 30/57
60/16 18/58
< 0.001 < 0.001
1 vs. 2§, 1 vs. 3§ 1 vs. 2§, 1 vs. 3§
204/26 91/139
*Non-normal distribution; †overall differences between groups; ‡significant difference from groups (§P < 0.01; ¶P < 0.05).
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Table 3 Regression analysis assessing the associations between pre-hospital delay and risk factors
Odds ratio
95% CI of odds ratio
Previous ulcers No 1.45 0.84–2.53 Yes Reference Medical insurance No 1.07 0.55–2.09 Yes Reference Housing conditions Bad 1.74 0.23–13.28 Moderate 0.59 0.18–1.87 Good Reference Income level Low 1.70 0.41–7.03 Moderate 2.41 0.79–7.39 High Reference Educational level Primary school 1.19 0.43–3.26 Secondary school 1.13 0.48–2.69 University Reference Performance of foot inspection Seldom 2.27 0.81–6.37 Sometimes 1.78 0.93–3.42 Usually Reference Diabetic clinic visits < 1 per year 1.35 0.42–4.26 1–2 per year 1.11 0.57–2.17 > 2 per year Reference Foot education received No 2.70 1.03–7.06 Yes Reference Knowledge of foot lesion danger signals No 2.14 1.16–3.94 Yes Reference
P
0.182
0.836
0.595 0.366
0.461 0.124
0.738 0.774
0.121 0.082
0.613 0.756
0.043
0.015
behaviours and more diabetic foot problem knowledge were associated with a short pre-hospital delay. The UK National Institute for Health and Clinical Excellence (NICE) (now known as the National Institute for Health and Care Excellence) recommends referral of patients with diabetic foot problems to a multidisciplinary foot care team within 24 h of the initial examination of the patient’s feet [17]. However, the availability of this strategy was limited because the majority (71.5%) of patients were admitted to the hospital 1 week after symptom onset in our study. Additionally, our findings suggest that a long pre-hospital delay is a major contributor to the morbidity of patients with diabetic foot problems, because a significant number of individuals who delay seeking care develop potentially preventable complications. This finding agrees with two other studies [9,18], which observed that a long pre-hospital delay contributed to deteriorating diabetic foot problems and resulted in amputation and mortality. Mild diabetic foot problems can progress to severe limb-threatening infection, sepsis and gangrene when these conditions are untreated, thereby putting the patients at increased risk for wound-related amputation and death [9]. Additionally, persistent inflammation and long-term fluctuating blood sugar levels can trigger cardiovascular events and increase
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the potential for death caused by ischaemic heart disease [19]. Patients with a history of myocardial infarction or stroke generally have a shorter pre-hospital delay among patients with acute coronary syndrome [20,21]. We found a similar result: patients with a history of foot ulcers also had a shorter pre-hospital delay than those without these events. Because pre-hospital delay reflects the patient’s own decision-making process, a previous ulcer or limb-threatening event might have led to greater symptom awareness, efficient evaluation and quicker decision making. However, Mantey et al. [22] did not detect any such relationship, possibly because of a different definition of ‘delay’ or a different study design. The decision to seek treatment is heavily influenced by the patient’s social context, cognitive process and economic situation, but these delay factors have not been fully explored. Lower socio-economic status prolongs pre-hospital delay time in patients with acute coronary syndrome [21,23]. Our findings show that lack of medical insurance, poor housing conditions, low income and low educational level were associated with a long pre-hospital delay in patients with diabetic foot problems. Although few researchers have studied the association between socio-economic status and pre-hospital delay time in patients with diabetic foot problems, Weng et al. [24] demonstrated that low socio-economic status was linked to increased morbidity and premature mortality in people with diabetes. One possible explanation is that patients with low socio-economic status do not seek medical care because they lack access, either physically or financially, to health care; another explanation is that patients with a low level of education lack vital knowledge and sensitivity about their illness and its consequences. Patients who receive education and training in the diabetic foot care programme have learned to seek immediate medical assistance when they find lesions on their feet [25]. In this study, diabetic foot education and knowledge of foot lesion danger signals were independently associated with pre-hospital delay. We stress the importance of providing education and information on self-care behaviours in diabetic foot problems. Patients with diabetic foot problem knowledge often have sufficient information about the recognition, causes, symptoms, management and consequences of diabetic foot problems. Therefore, patients with diabetic foot problem knowledge are fully prepared to self-manage tasks, such as following up regularly, inspecting their feet frequently, detecting foot problems promptly, and seeking early and immediate medical care.
Conclusions There are significant and potentially modifiable factors for pre-hospital delay in patients with diabetic foot problems. These delays are most marked in patients who have no previous history of foot problems, no medical insurance, poor housing conditions, low income, low levels of
ª 2013 The Authors. Diabetic Medicine ª 2013 Diabetes UK
Research article
education, infrequent foot inspections, few follow-up medical visits, no diabetic foot education and lack of knowledge of foot lesion danger signals. A long pre-hospital delay is likely to contribute significantly to these poorer outcomes, lower-extremity amputation and mortality. We recommend developing a community intervention programme targeting at-risk communities to encourage earlier assessment by a multidisciplinary team to reduce disparity and improve foot outcomes in patients with diabetes.
Limitations
First, this study used arbitrary cut-off scores based on the 33rd and 66th percentiles to differentiate between short and long pre-hospital delays. However, there is no standard criterion on short or long pre-hospital delay times in the literature. Second, the data set used in this study was generated from one hospital, limiting its generalizability to other hospitals; therefore, additional large-scale research is needed. Third, the exclusion criteria may have introduced a bias because the patients who had communication problems and refused to participate in the study often demonstrated poor compliance, which may have caused delays in the detection of their foot problems and led to their delayed admission. Finally, retrospective surveys have inherent deficiencies. A prospective design would be preferable to establish the direction of causality.
Funding
This study was funded by the National Key Clinical Department Construction Project.
Competing interests
None declared.
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