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Pathophysiology/Complications
ORIGINAL ARTICLE
Amputation and Mortality in New-Onset Diabetic Foot Ulcers Stratified by Etiology
PROBAL K. MOULIK, MRCP1 ROBERT MTONGA, MB2 GEOFFREY V. GILL, MD1
OBJECTIVE -- Foot ulcers and their complications are an important cause of morbidity and mortality in diabetes.Diabetes Care 12:24 -31, 1989
Apelqvist J, Ragnarson-Tennvall G, Pers- son U, Larsson J: Diabetic foot ulcers in a multidisciplinary setting: an economic analysis of primary healing and healing with amputation.Med Clin North Am 82:949 -971, 1998 Maser RE, Nielsen VK, Bass EB, Manjoo Q, Dorman JS, Kelsey SF, Becker DJ, Or- chard TJ: Measuring diabetic neuropathy: assessment and comparison of clinical ex- amination and quantitative sensory test- ing.Adler AI, Boyko EJ, Ahroni JH, Smith DG: Lower-extremity amputation in diabetes: the independent effects of peripheral vas- cular disease, sensory neuropathy, and foot ulcers.Diabet Foot 5:51-53, 2002
Bild DE, Selby JV, Sinnock P, Browner WS, Braveman P, Showstack JA: Lower- extremity amputation in people with dia- betes: epidemiology and prevention.Cardiac and cerebrovascular diseases ac- counted for the majority of deaths (38%), followed by pneumonia (27%), emphy-
Patients (n) Age (years) Sex
Male
Female Diabetes
Type 1 Type 2 Unclassified
Ulcer type Neuropathic Ischemic Neuroischemic Other
Total 185
65 ?Tan JS, Friedman NM, Hazelton-Miller C, Flanagan JP, File TM: Can aggressive treatment of diabetic foot infections re- duce the need for above-ankle amputa- tion?A standard neurological examination tested the sensation to light touch (cotton wool), pain (sterile neuro- logical examination pins [Neurotips]), vi- bration (128-Hz tuning fork), and tendon reflexes at the ankle (3).Kaplan-Meier survival curves were generated for the cohort, and the log-rank test was used to test equality of survivor
Foot ulcers and their complications are an important cause of morbidity and mortality in patients with diabe-
tes.Boyko et al. (17) reported a relative risk of death of 2.39 among diabetic patients developing new foot ulcers and commented that overall high mortality in all the ulcer sub- types suggests that diabetic foot ulcers may serve as a marker of as-yet-unknown conditions increasing mortality.RamseySD,NewtonK,BloughD,McCul- loch DK, Sandhu N, Reiber GE, Wagner EH: Incidence, outcomes, and cost of foot ulcers in patients with diabetes.Peripheral vascular disease (PVD) was considered present when both the dorsalis pedis and poste- rior tibial pulses were absent in the af- fected limb (4).On multinomial regression analysis, among the variables, only age predicted mortality and none was independently re-
Table 2--Five-year amputation rates and time to amputation
Neuropathic (N) Neuroischemic (NI)
Ischemic (I)
Other 28
Cases
(n) (n)
83 30 44
Amputation
Time to amputation (months)
58 (55-61)
62 (58-65)* 54 (44-62) 52 (44-60)??We believe that those who developed ulcers in the absence of clinical neuropathy were
Moulik, Mtonga, and Gill
Cases (n)
Overall 185 Ulcer type
5-year mortality
Deaths Survival
(n) (months) (%)
52 50 (47-54) 44
Data are means (95% CI) unless noted otherwise.Mayfield JA, Reiber GE, Nelson RG, Greene T: A foot risk classification system to predict diabetic amputation in Pima In- dians.Anagnostopoulos D FA, Bates M, Doxford M, Wilson S, Edmonds ME: Mortality in diabetic foot ulcer patients: major differ- ence between ischaemic and neuropathic patients (Abstract).The present study aims to examine outcomes in patients with new-onset dia- betic foot ulcers of various etiologies with reference to amputations and mortality.Lee JS, Lu M, Lee VS, Russell D, Bahr C, Lee ET: Lower-extremity amputation: in- cidence, risk factors, and mortality in the Oklahoma Indian Diabetes Study.Boyko EJ, Ahroni JH, Smith DG, Dav- ignon D: Increased mortality associated with diabetic foot ulcer.The present study aims to examine the long-term outcome in terms of amputations and mortality in patients with new-onset diabetic foot ulcers in subgroups stratified by etiology.RESULTS -- Of the 185 patients studied, 41% had peripheral vascular disease (PVD) and 61% had neuropathy; 45%, 16%, and 24% of patients had neuropathic, ischemic, and neurois- chemic ulcers, respectively.Address correspondence and reprint requests to Dr. Probal K. Moulik, MRCP, Department of Diabetes, Flat 39, Coniston House, University Hospital Aintree, Liverpool, L9 7AL UK. E-mail: [email protected], on multi- variate forward stepwise Cox regression analysis to estimate time to outcome, age predicted shorter survival time (P ?However, mean age at presentation of ischemic ul- cer patients was about 8 years more than that of neuropathy patients, and on the multinomial regression analysis model, only increasing age was found to predict mortality.The mortality appears to be independent of factors increasing ulcer risk, i.e., neur- opathy and PVD, in patients with estab- lished diabetic foot ulcers.3):S61-S64, 1998
Carrington AL, Mawdsley SK, Morley M, Kincey J, Boulton AJ: Psychological status of diabetic people with or without lower limb disability.Diabe- tes 42:876 - 882, 1993
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Original text

Pathophysiology/Complications
ORIGINAL ARTICLE
Amputation and Mortality in New-Onset Diabetic Foot Ulcers Stratified by Etiology
PROBAL K. MOULIK, MRCP1 ROBERT MTONGA, MB2 GEOFFREY V. GILL, MD1
OBJECTIVE — Foot ulcers and their complications are an important cause of morbidity and mortality in diabetes. The present study aims to examine the long-term outcome in terms of amputations and mortality in patients with new-onset diabetic foot ulcers in subgroups stratified by etiology.
RESEARCH DESIGN AND METHODS — Patients presenting with new ulcers (dura- tion ?1 month) to a dedicated diabetic foot clinic between 1994 and 1998 were studied. Outcomes were determined until March 2000 (or death) from podiatry, hospital, and district registers. Baseline clinical examination was done to classify ulcers as neuropathic, ischemic, or neuroischemic. Five-year amputation and mortality rates were derived from Kaplan-Meier sur- vival analysis curves.
RESULTS — Of the 185 patients studied, 41% had peripheral vascular disease (PVD) and 61% had neuropathy; 45%, 16%, and 24% of patients had neuropathic, ischemic, and neurois- chemic ulcers, respectively. The mean follow-up period was 34 months (range 1– 65) including survivors and patients who died during the study period. Five-year amputation rates were higher for ischemic (29%) and neuroischemic (25%) than neuropathic (11%) ulcers. Five-year mortal- ity was 45%, 18%, and 55% for neuropathic, neuroischemic, and ischemic ulcers, respectively. Mortality was higher in ischemic ulcers than neuropathic ulcers. On multivariate regression analysis, only increasing age predicted shorter survival time.
CONCLUSIONS — All types of diabetic foot ulcers are associated with high morbidity and mortality. The increased mortality appears to be independent of factors increasing ulcer risk— that is, neuropathy and PVD—in patients with established foot ulcers.
The present study aims to examine outcomes in patients with new-onset dia- betic foot ulcers of various etiologies with reference to amputations and mortality.
RESEARCH DESIGN AND METHODS — Patients were recruited from the Diabetic Foot Clinic at Univer- sity Hospital Aintree in Liverpool be- tween 1994 and 1998. All patients with newly diagnosed diabetic foot ulcers (du- ration ?1 month) were enrolled. A chi- ropodist and a consultant diabetologist assessed all the patients.
Diabetes was defined as type 1 if the age of onset was ?30 years and insulin treatment was started at diagnosis. Pa- tients with onset of diabetes after age 30 years and initially on diet or oral hypogly- cemic therapy were considered to have type 2 diabetes. A foot ulcer was defined as a full-thickness skin defect present for at least 2 weeks. A standard neurological examination tested the sensation to light touch (cotton wool), pain (sterile neuro- logical examination pins [Neurotips]), vi- bration (128-Hz tuning fork), and tendon reflexes at the ankle (3). Peripheral neu- ropathy was considered present if three of the four were absent. Peripheral vascular disease (PVD) was considered present when both the dorsalis pedis and poste- rior tibial pulses were absent in the af- fected limb (4). Based on this, ulcers were classified as neuropathic, ischemic, or neuroischemic.
Data on outcome were collected from podiatric and hospital records and district registers up to March 2000 (or death, if earlier). Mortality and lower-extremity amputation events were noted on all the patients from the above sources. Amputa- tion included both major and minor pro- cedures including toe amputations. Statistical analysis was performed using SPSS for Windows (SPSS, Chicago, IL). The unpaired t test was used for mean values and the ?2 test for categorical val- ues. Kaplan-Meier survival curves were generated for the cohort, and the log-rank test was used to test equality of survivor
Foot ulcers and their complications are an important cause of morbidity and mortality in patients with diabe-
tes. Annual incidence of foot ulcers is 1% to 4% and prevalence 5% to 10% in pa- tients with diabetes (1). About 50% of pa- tients undergoing nontraumatic lower- limb amputations have diabetes (2). These patients have a high mortality fol- lowing amputation, ranging from 39% to 80% at 5 years (1).
Diabetes Care 26:491–494, 2003
There are relatively few studies on survival of patients with diabetic foot ul- cers. Furthermore, many of these studies are based on prevalent cases, which over- estimate mortality because ulcers are likely to have been present for months to years before the patients are enrolled. Fi- nally, little is known about the survival of patients with different types of foot ulcers, i.e., neuropathic, neuroischemic, or isch- emic.
●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●
From the 1Department of Diabetes, University Hospital Aintree, Liverpool, U.K.; and the 2Department of Medicine, Ndola Central Hospital, Ndola, Zambia.
Address correspondence and reprint requests to Dr. Probal K. Moulik, MRCP, Department of Diabetes, Flat 39, Coniston House, University Hospital Aintree, Liverpool, L9 7AL UK. E-mail: [email protected].
Received for publication 19 May 2002 and accepted in revised form 31 October 2002.
Abbreviations: PVD, peripheral vascular disease.
A table elsewhere in this issue shows conventional and Syste`me International (SI) units and conversion
factors for many substances.
DIABETES CARE, VOLUME 26, NUMBER 2, FEBRUARY 2003
491


Outcome in diabetic foot ulcers
functions between the various groups. Multinomial and forward stepwise Cox linear regression analysis was used to test for associations between risk factors and outcomes.
RESULTS — Between 1994 and 1998, a total of 185 patients with new ulcers were seen at the Diabetic Foot Clinic (Fig. 1). Of these patients, 118 (64%) were male. The mean age (? SD) at presenta- tion was 65 ? 13 years (range 25–93). The majority of patients had type 2 diabe- tes (84%), whereas 10% had type 1 dia- betes (in the remaining 6%, diabetes type was uncertain from the records). Neurop- athy and PVD were present in 113 (61%) and 76 (41%) patients, respectively. Based on this, ulcers were classified as neuropathic, ischemic, and neuroisch- emic in 83 (45%), 44 (24%), and 30 (16%) subjects, respectively. In 28 pa- tients (15%), there was neither clinical neuropathy nor PVD by the study criteria (Table 1).
The median follow-up period was 28 months (range 1–65), including survi- vors and patients who died during the study period. A total of 30 patients (17%) had amputations, giving a crude amputa- tion rate of 16%. Mean time free of ampu- tation was 58 months, and the 5-year amputation rate was 19% for the whole group. Patients with PVD had a signifi- cantly higher 5-year amputation rate than those without PVD (P ? 0.02). The 5-year amputation rates were higher for isch- emic (29%) and neuroischemic (25%) ul- cers than neuropathic ulcers (11%) (Table 2 and Fig. 2).
Mortality trends were also assessed in
Table 1—Characteristics at baseline of patients in relation to subsequent mortality
Figure 1—Number of pa- tients and outcomes (data on outcome until March 2000).
be older at presentation (mean age 71 ? 10 years) than those remaining alive (63 ? 13 years; P ? 0.01). Mortality rates remained similar in both sexes and types of diabetes (Table 1). Again, patients with PVD and ischemic ulcers had a signifi- cantly worse outcome, with a mean sur- vival period of 41 months and a 5-year mortality rate of 56%. Five-year mortality was higher in patients who had amputa- tion (47%) than in those without (43%), though this was not statistically signifi- cant (Table 3 and Fig. 3)
Cause of death could be ascertained in 26 patients who died in our hospital. Cardiac and cerebrovascular diseases ac- counted for the majority of deaths (38%), followed by pneumonia (27%), emphy-
Patients (n) Age (years) Sex
Male
Female Diabetes
Type 1 Type 2 Unclassified
Ulcer type Neuropathic Ischemic Neuroischemic Other
Total 185
65 ? 13 118
67
19 155 11
83 44 30 28
Alive (%) 133 (72)
63 ? 13 83 (70)
50 (75)
14 (74) 110 (71) 9 (82)
62 (75) 24 (55) 24 (80) 23 (82)
Dead (%) 52 (28)
71 ? 10* 53 (30)
17 (25)
5 (26) 45 (29) 2 (18)
21 (25) 20 (46) 6 (20) 5 (18)
Data are n (%) or means ? SD. P ?0.01.
the same period. Fifty-two patients had died, the mean survival period being 50 months and the 5-year mortality rate 44% for the entire group. Patients who died during subsequent follow-up tended to
sema (8%), malignancy (12%), septice- mia (12%), and renal failure (4%).
On multinomial regression analysis, among the variables, only age predicted mortality and none was independently re-
Table 2—Five-year amputation rates and time to amputation
Neuropathic (N) Neuroischemic (NI)
Ischemic (I)
Other 28
Cases
(n) (n)
83 30 44
Amputation
Time to amputation (months)
58 (55–61)
62 (58–65)
54 (44–62) 52 (44–60)‡§ 50 (44–55)
5-year amputation rate (%)
19
11† 25 29§ 22?
Overall 185 Ulcer type
30
8
7 11 4
Data are means (95% CI) unless noted otherwise. *P ? 0.06 for N vs. NI; †P ? 0.05 for N vs. NI; ‡P ? 0.06 for N vs. I; §P ? 0.05; ?four-year amputation rate.
492
DIABETES CARE, VOLUME 26, NUMBER 2, FEBRUARY 2003


lated to amputation. Similarly, on multi- variate forward stepwise Cox regression analysis to estimate time to outcome, age predicted shorter survival time (P ? 0.01).
CONCLUSIONS— Footproblemsin diabetes continue to challenge the clini- cians who care for these patients. Not only are they associated with morbidity and disability, but they also lead to significant impairment of quality of life (5). Although a high mortality is well documented in patients with diabetic foot problems fol- lowing amputation, few studies have as- sessed long-term mortality in patients with new-onset diabetic foot ulcers (6).
The study design included only pa- tients with recent-onset foot ulcers, thus avoiding overestimation of disease sever- ity that may occur when prevalent cases are included. We used simple clinical tests to diagnose PVD and neuropathy. These can be easily performed in any hos- pital or community foot clinic. We regard our results as robust, since a large number of patients with foot ulcers were followed for a substantial period. Mortality rates are likely to be particularly accurate, as we included podiatry records, hospital data, and information from the district mortal- ity register. However, the exact cause of death could be ascertained only if the pa- tient died in our hospital.
Observational studies suggest that 6–43% of patients with diabetes and a foot ulcer eventually progress to amputa- tion (7–9). Ramsey et al. (10) reported
Table 3—Mean survival period and 5-year mortality
Neuropathic (N) Neuroischemic (NI) Ischemic (I)
Other
Amputation No amputation
83 21 30 6 44 20 28 5 30 9
153 43
52 (48–57) 45 53 (45–61)* 20 41 (34–49)†‡ 56†‡ 46 (42–51) 23§ 50 (42–58) 47 50 (46–54) 43
Figure 2—Cumulative amputa- tion rates in foot ulcers of various etiologies.
amputation rates of 11.2% in patients with new-onset foot ulcers over a 4-year period. This is in agreement with crude amputation rates (16%), 5-year amputa- tion rates (19%), and mean time to ampu- tation (58 months) in our series. Absence of peripheral pulses has been established to be a risk factor for subsequent ampu- tation (11–16). In our study, 59% of pa- tients who had amputations had PVD. Five-year amputation rates (27%) were higher, and time to amputation (53 months) was less (P ? 0.05) in these pa- tients. Prevalence of peripheral neuropa- thy was not significantly more common among amputees. Indeed, time to ampu- tation was greater in those with neuropa- thy than in those without (Table 2). We believe that those who developed ulcers in the absence of clinical neuropathy were
Moulik, Mtonga, and Gill
Cases (n)
Overall 185 Ulcer type
5-year mortality
Deaths Survival
(n) (months) (%)
52 50 (47–54) 44
Data are means (95% CI) unless noted otherwise. *P ? 0.05 for I vs. NI; †P ? 0.05 for I vs. N; †P ? 0.05; §three-year mortality.
Figure 3— Cumulative survival rates in foot ulcers of various eti- ologies.
DIABETES CARE, VOLUME 26, NUMBER 2, FEBRUARY 2003
493


Outcome in diabetic foot ulcers
more likely to have PVD as a confounding variable.
Patients with foot ulcers were noted to have high mortality rates in our study (mean survival period 50 months and 5-year mortality rate 44%). Boyko et al. (17) reported a relative risk of death of 2.39 among diabetic patients developing new foot ulcers and commented that overall high mortality in all the ulcer sub- types suggests that diabetic foot ulcers may serve as a marker of as-yet-unknown conditions increasing mortality. Most au- thors have found higher mortality in dia- betic patients with previous amputation (8,11,18). In our series, five-year mortal- ity among amputees (47%) was not sig- nificantly greater than among those without amputation (43%). Like us, Ram- sey et al. (10) did not find higher mortal- ity among 80 patients who had amputations in a group of 514 patients with diabetic foot ulcers.
Few studies have addressed the issue of survival among patients with different types of diabetic foot ulcers. In a cohort of diabetic patients having local foot sur- gery, only 11% of those with arteriopathy, versus 58% of those without PVD, sur- vived after a median follow-up of 92 months (19). Similar results were noted in a study at King’s College, London (20). In our study, patients with ischemic ul- cers had a higher 5-year mortality (56%) than those with neuropathy (45%; P ? 0.01). Indeed, on paired comparisons in our and most other series, presence of PVD is significantly associated with re- duced survival in foot ulcer patients (17– 20). This is likely to be due to associated atherosclerotic vascular disease in the cor- onary and cerebral circulations. However, mean age at presentation of ischemic ul- cer patients was about 8 years more than that of neuropathy patients, and on the multinomial regression analysis model, only increasing age was found to predict mortality. Thus, the higher age of patients with ischemic ulcers acts as a confound- ing variable.
Three-year mortality and amputation rates of 23% and 22%, respectively, were noted among patients who did not have neuropathy or PVD. It is likely that these
patients had underlying PVD or neurop- athy not detected by the clinical criteria. Either way, our results prove that any pa- tient with a diabetic foot ulcer is at high risk of amputation and death irrespective of underlying etiology and deserves ag- gressive management.
In summary, this study confirms the high mortality of patients with diabetic foot ulcers in addition to the associated substantial morbidity and disability. The mortality appears to be independent of factors increasing ulcer risk, i.e., neur- opathy and PVD, in patients with estab- lished diabetic foot ulcers. An aggressive multidisciplinary approach is warranted not only to manage foot problems in such patients but also to recognize and reduce risk of death from other comorbid condi- tions to save both limb and life.
References
9. Tan JS, Friedman NM, Hazelton-Miller C, Flanagan JP, File TM: Can aggressive treatment of diabetic foot infections re- duce the need for above-ankle amputa- tion? Clin Infect Dis 23:286 –291, 1996
10. RamseySD,NewtonK,BloughD,McCul- loch DK, Sandhu N, Reiber GE, Wagner EH: Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 22:382–387, 1999
11. Lee JS, Lu M, Lee VS, Russell D, Bahr C, Lee ET: Lower-extremity amputation: in- cidence, risk factors, and mortality in the Oklahoma Indian Diabetes Study. Diabe- tes 42:876 – 882, 1993
12. New JP, McDowell D, Burns E, Young RJ: Problem of amputations in patients with newly diagnosed diabetes mellitus. Diabet Med 15:760 –764, 1998
13. Deerochanawong C, Home PD, Alberti KG: A survey of lower limb amputation in diabetic patients. Diabet Med 9:942–946, 1992
14. Adler AI, Boyko EJ, Ahroni JH, Smith DG: Lower-extremity amputation in diabetes: the independent effects of peripheral vas- cular disease, sensory neuropathy, and foot ulcers. Diabetes Care 22:1029 –1035, 1999
15. Lehto S, Ronnemaa T, Pyorala K, Laakso M: Risk factors predicting lower extremity amputations in patients with NIDDM. Di- abetes Care 19:607– 612, 1996
16. Mayfield JA, Reiber GE, Nelson RG, Greene T: A foot risk classification system to predict diabetic amputation in Pima In- dians. Diabetes Care 19:704 –709, 1996
17. Boyko EJ, Ahroni JH, Smith DG, Dav- ignon D: Increased mortality associated with diabetic foot ulcer. Diabet Med 13: 967–972, 1996
18. Faglia E, Favales F, Morabito A: New ulceration, new major amputation, and survival rates in diabetic subjects hospi- talized for foot ulceration from 1990 to 1993: a 6.5-year follow-up. Diabetes Care 24:78 – 83, 2001
19. Campbell WB, Ponette D, Sugiono M: Long-term results following operation for diabetic foot problems: arterial disease confers a poor prognosis. Eur J Vasc Endo- vasc Surg 19:174 –177, 2000
20. Anagnostopoulos D FA, Bates M, Doxford M, Wilson S, Edmonds ME: Mortality in diabetic foot ulcer patients: major differ- ence between ischaemic and neuropathic patients (Abstract). Diabetologia 42:A311, 1999
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Reiber GE: Epidemiology of Foot Ulcerations and Amputations in Diabetes, 6th ed. St. Louis, MO, Mosby, 2001
Slovenkai MP: Foot problems in diabetes. Med Clin North Am 82:949 –971, 1998 Maser RE, Nielsen VK, Bass EB, Manjoo Q, Dorman JS, Kelsey SF, Becker DJ, Or- chard TJ: Measuring diabetic neuropathy: assessment and comparison of clinical ex- amination and quantitative sensory test- ing. Diabetes Care 12:270 –275, 1989 Gadsby R, McInnes A: The at-risk foot: the role of the primary care team in achieving St Vincent targets for reducing amputation. Diabetic Medicine 15 (Suppl. 3):S61–S64, 1998
Carrington AL, Mawdsley SK, Morley M, Kincey J, Boulton AJ: Psychological status of diabetic people with or without lower limb disability. Diabetes Res Clin Pract 32: 19 –25, 1996
Moulik PK, Gill GV: Mortality in diabetic patients with foot ulcers. Diabet Foot 5:51–53, 2002
Bild DE, Selby JV, Sinnock P, Browner WS, Braveman P, Showstack JA: Lower- extremity amputation in people with dia- betes: epidemiology and prevention. Diabetes Care 12:24 –31, 1989
Apelqvist J, Ragnarson-Tennvall G, Pers- son U, Larsson J: Diabetic foot ulcers in a multidisciplinary setting: an economic analysis of primary healing and healing with amputation. J Intern Med 235:463– 471, 1994
494
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