- Email: [email protected]
Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital
G Model DSX 854 No. of Pages 4
Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Diabetes & Metabolic Syndrome: Clinical Research & Reviews journal homepage: www.elsevier.com/locate/dsx
Original Article
Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital Ramya Kateela , Alfred J. Augustineb , Shivananda Prabhub , Sheetal Ullalc, Manohar Paib , Prabha Adhikarid,* a
Department of Medicine, Manipal University, Mangalore, India Department of Surgery, Manipal University, Mangalore, India Department of Pharmacology, Manipal University, Mangalore, India d Department of Medicine, Yenepoya University, Deralakatte, Mangalore, India b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 August 2017 Accepted 20 August 2017 Available online xxx
Aim: To evaluate the clinical and microbiological profile of diabetic foot ulcer patients admitted to a tertiary care hospital. Methodology: This study recruited 120 diabetic foot ulcer patients of all grade. Their medical records were evaluated retrospectively. Results: We found that median age of patient was 60(52, 67.75) years. 68.3% of patients were males. Median duration of diabetes mellitus was 15(10, 20) years. Mean HbA1C and fasting glucose was 10.3 2.3 and 167.6 52.42 respectively. Neuropathy (35%) and peripheral vascular disease (23.3%) was major micro vascular and macro vascular complication associated. Different locations of ulcers were toe (23.3%), sole (20%), dorsum (18.3%), shin (16.6%), heel (13.3%), and ankle (8.3%). Bacterial infection was seen in 81.66% patients out of which 23.3% had poly microbial infection. Conclusion: Diabetic foot ulcer patient had poor blood glucose control with elevated HbA1C and fasting blood glucose level. Neuropathy and peripheral vascular disease, hypertension were major complications. Staphylococcus aureus, Pseudomonas aeruginosa were common infecting bacteria. © 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Keywords: Diabetic foot ulcer Complications of diabetes Bacterial infection of foot
1. Introduction The incidence of diabetes mellitus is increasing at an alarming rate along with the complications associated with it. The WHO has estimated that the global prevalence of diabetes has increased from 4.75% in 1980 to 8.5% in 2014 [1]. Diabetes mellitus is associated with several complications. Diabetic foot ulcer is one such complication which has a significant impact on the quality of life of the patient and on the associated health care burden. It is one of the common causes of morbidity, hospital admission and amputation among diabetics. In the clinical population of India, prevalence of diabetic foot ulcer is found to be 3.6% [2]. The approximate lifetime risk of a diabetic patient developing an ulcer is 25% [3,4]. As reported in a south Indian study, patients with diabetes spend 9.3% of their total income towards treatment whereas patients with diabetes and foot ulcer spent 32.3% of their
* Corresponding author. E-mail address: [email protected] (P. Adhikari).
total income towards treatment [5]. Hence diabetic foot ulcer can be considered as an economic and medical threat in health care system. The treatment of diabetic foot ulcer includes multiple approaches. Hence studying about the profile of patients who develop foot ulcers, extent of the disease and the complications associated with it will help health care providers to plan better prevention programs and treatment strategies. Also clinical profile of a disease varies in different geographical area. Hence studying clinical profile of local population will help in better prevention and treatment of a disease. With the above background the present study was undertaken to evaluate the clinical and microbiological profile of diabetic foot ulcer patients. 2. Materials and methods Institutional ethics committee permission was obtained for conduct of the study. Medical records of 120 diabetic patients with foot ulcer were retrieved and reviewed. Patients’ demographic data, associated micro vascular and macro vascular complications,
http://dx.doi.org/10.1016/j.dsx.2017.08.008 1871-4021/© 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
2
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
laboratory values like fasting blood glucose level, glycosylated hemoglobin level, duration of diabetes mellitus, location of ulcer and microbial infection details were noted down. 3. Results Table 1 shows patient’s demographic data, duration diabetes and laboratory values. Graph 1 shows number of patients affected with micro vascular complications like neuropathy, nephropathy and retinopathy. All three micro vascular complication was present in 15%(18) patients. Graph 2 shows the number of patients associated with macro vascular complications like coronary artery disease, cerebrovascular disease and peripheral vascular disease. Hypertension, dementia, dyslipidemia and congestive heart failure were other important complications associated. Table 2 shows the no of patients affected with these complications. Aerobic bacterial infection was seen in 81.66%(98) patients out of which 28.5%(28) patients had poly microbial infection. Table 3 shows different bacteria isolated from diabetic foot ulcer. Graph 3 shows location of ulcer in patient’s foot.
Graph 1. Micro vascular complications associated.
4. Discussion Diabetic foot is one of the most common devastating complications among other chronic complications of diabetes mellitus. It is the leading cause of non traumatic amputation throughout the world [6]. There are multiple factors which lead to development of foot ulcer in diabetic patients which may even result in amputation if not treated. In our study we found that median age of patients was 60(52, 67.75). The proportion of diabetic foot ulcer varied between 1.7 and 3.3% in younger patients and 5 and 10% among older patients, which is similar to previous studies. Old age was considered one of the independent risk factors for the development of diabetic foot ulcer. Risk of ulceration increases two to four fold with age in diabetes [7,8]. Most of the earlier studies have shown a higher rate of diabetic foot among males. Similarly in our study more number of male patients (68%) had diabetic foot ulcer compared to females (32%). This may be because females have less severe neuropathy, increased joint mobility, low foot pressure and better propensity towards self-care compared to men. In addition males are more likely to be exposed to trauma and wear improper foot wear especially in the Indian scenario [9,10]. Another important common risk factor identified for the development of foot ulcer in diabetic patients is longer duration of diabetes mellitus and uncontrolled blood sugar level. In our study median duration of diabetes was 15 years (10, 17) and mean HbA1c and FBS was 10.3 2.3% and 167.6 52.42 mg/dl respectively. Longer the duration of diabetes, more is the micro and macro vascular complications associated with it which in turn
Graph 2. Macro vascular complications associated.
Table 2 Other important complications associated. Complication
Percentage (N)
Hypertension Dyslipidemia Congestive heart failure Dementia
58.3%(70) 15%(12) 11.7%(14) 5%(6)
Table 3 Bacteria Isolated. Bacteria
Percentage (N)
Staphylococcus aureus E. coli Pseudomonas aeruginosa Klebsiella species Proteus species Enterococcus species Streptococcus
40.81%(40) 34.69%(34) 30.61%(30) 12.63%(12) 5.10%(5) 5.10%(5) 1.02%(1)
Table 1 Patients’ demographic and other details. Parameter
Value
Median age (IQR) in years Gender ratio% (n = 120)
60(52,67.75) Male 68% (82) 15(10,17) 10.3 2.3 167.6 52.42 Grade 1 43.3%(52)
Median Duration of diabetes mellitus in years (IQR) Mean HbA1C SD (%) Mean Fasting blood glucose SD(mg/dl) Ulcer grade
Female 32%(38)
Grade 2 46.6%(56)
Grade 3 10%(12)
Grade 4 0
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
Graph 3. Location of ulcer.
results in ulceration of foot and amputation. Studies have shown that patients with a poor glycemic control have a 2–4 fold increased risk of ulceration [7,11]. The most commonly stated microvascular complication which is a risk factor for development of diabetic foot is neuropathy. In our study 35% of patients had neuropathy. Several studies have shown that prevalence of neuropathy in diabetic foot ulcer varies from 8% to 59% [12–15] but it is also reported that Asians have relatively lower diabetic foot complications and amputations compared to Europeans. One of the proposed reason for this is Asians have reduced prevalence of diabetic neuropathy and peripheral artery disease compared to Europeans [16–18]. In our study we found that 25% of diabetic foot ulcer patients had nephropathy. Incidence of diabetic foot ulcer increases with progressive renal impairment. Patients with both diabetes and chronic kidney disease have two to six times risk of getting lower extremity amputation compared to patient with only diabetes. Most studies have claimed atherosclerosisas a common factor and noted an association between peripheral vascular disease and chronic kidney disease [19]. But in our study only 32% of patients who had nephropathy had peripheral vascular disease. These results are similar to those of David J et al. who in their study showed an association between chronic kidney disease and diabetic foot ulcer and lower extremity amputation. This association was present even without clinically apparent peripheral vascular disease. They hypothesized that chronic kidney disease can be used as an early marker for diabetic foot ulcer because hyperglycemia in cells leads to renal damage first, since renal cells are most sensitive and cannot replenish. Skin is affected later which can replenish from neighbouring cells, transient amplifying cells local to the wound and bone marrow–derived cells [20]. Hence we infer that poor glycemic control is the main culprit leading to diabetic nephropathy at first and diabetic foot later. Studies have also found a significant association between diabetic foot ulcer and retinopathy. It can be used as a proxy for severity of diabetes [21]. Decreased vision is one of the risk factors for the development of diabetic foot ulcer. In diabetic retinopathy patient’s decreased vision may lead to trauma and patient may not
3
be able to examine the foot properly [22]. In our study 28.3% patients had retinopathy. Peripheral vascular disease is another commonly stated risk factor for the development of diabetic foot ulcer. In our study 38.5% of patients had peripheral vascular disease. It also increases the risk of lower extremity amputation by delaying healing process. It is also associated with increased incidence of cardiovascular and cerebrovascular events. In our study 26.75% of patients had cardiovascular disease and 3.3% of patients had cerebrovascular events. Hence it is important to diagnose peripheral vascular disease in diabetic patients in order to take early prevention measures to avoid foot ulcer, cardiovascular events and also mortality. In patients with diabetic foot ulcer early recognition and expert assessment are required to determine the need for revascularization to promote ulcer healing [23]. Another important risk factor we observed in our study was hypertension. 58.3% of diabetic foot ulcer patients had hypertension. Studies have shown that approximately 75% of diabetic patients have hypertension. There is a significant amount of overlap between complications of diabetes and hypertension. It is considered one of the risk factors for lower extremity amputation [24]. Previous studies showed that people with diabetes mellitus have a twofold higher risk of developing dementia [25]. Amputation, micro vascular disease and poor glycemic control were associated with impaired cognitive function [26]. But in our study only 4% of patients had dementia. In our study Pseudomonas Sps., Staphylococcus aureus and E. coli were the commonly isolated aerobic bacteria. These results are similar to previous studies [27–31]. 5. Conclusion In our study we noted that diabetic foot ulcer patients had prolonged duration of diabetes with poor blood glucose control. Along with neuropathy and peripheral vascular disease hypertension, nephropathy, retinopathy and coronary artery disease were major complications associated. Most of the wounds were infected with Pseudomonas sps., Staphylococcus aureus and E. coli. Hence treating diabetic foot ulcer requires a multidisciplinary team consisting of a podiatrist, dialectologist, a vascular surgeon, infectious disease specialist, neurologist in order to address all the complications associated, so that incidence of lower extremity amputation reduces. Conflicts of interest Authors declare no conflict on interest. References [1] http://www.who.int/mediacentre/factsheets/fs312/en/. (Accessed 3 March 2017). [2] Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcer in patients with diabetes. JAMA 2005;293:217–28. [3] International Working Group on the Diabetic Foot. Epidemiology of Diabetic Foot Infections in a Population Based Cohort. Noordwijkerhout, the Netherlands: International Working Group on the Diabetic Foot; 2003. [4] Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJM. Diabetic foot syndrome: evaluating the prevalence and incidence of foot pathology in Mexican Americans and non-Hispanic whites from a diabetes disease management cohort. Diabetes Care 2003;26:1435–8. [5] Shobhana R, Rama Rao P, Lavanya A, Vijay V, Ramachandran A. Cost burden to Diabetic patients with foot complications- a study from Southern India. JAPI 2000;48:12. [6] Frykberg RG, Armstrong DG, Giurini J, Edwards A, Kravette M, Kravitz S, et al. Diabetic foot disorders: a clinical practice guideline. American College of Foot and Ankle Surgeons. J Foot Ankle Surg 2000;39(S5):S1–S60. [7] Reiber GE, Ledoux WR. Epidemiology of Diabetic Foot Ulcers and Amputations: Evidence for Prevention the Evidence Base for Diabetes Care. John Wiley &
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
4
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
[8]
[9] [10] [11]
[12]
[13]
[14]
[15] [16]
[17]
[18]
Sons, Ltd; 2003. p. 641–65. . Available: http://dx.doi.org/10.1002/0470846585. ch28. Khalid AR, Mohammad AD, Samir O, Amira MY, Shazia NS, Heba MI, et al. Diabetic foot complications and their risk factors from large retrospective cohort study. PLoS One 2015;10(5):e0124446. Monica E. Gender difference in diabetes-related lower extremity amputations. Clin Orthop Relat Res 2011;469(July (7)):1951–5. Dinh T, Veves A. The influence of gender as a risk factor in diabetic foot ulceration. Wounds 2008;20(May (5)):127–31. Jyothilekshmy V, Arun SM, Abraham Suja. Epidemiology of diabetic foot complications in podiatry clinic of a tertiary hospital in south India. Indian J Health Sci 2015;8(1):48–51. Young MJ, Boulton AJ, MacLeod AF, Williams DR, Sonksen PH. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993;36:150–4. Partanen J, Niskanen L, Lehtinen J, Mervaala E, Siitonen O, Uusitupa M. Natural history of peripheral neuropathy in patients with non-insulin-dependent diabetes mellitus. N Engl J Med 1995;333:89–94. Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology 199343: 817–817. Deli G, Bosnyak E, Pusch G, Komoly S, Feher G. Diabetic neuropathies: diagnosis and management. Neuroendocrinology 2013;98:267–80. Abbott CA, Garrow AP, Carrington AL, Morris J, Van Ross ER, Boulton AJ, et al. Foot ulcer risk is lower in South-Asian and African-Caribbean compared with European diabetic patients in the UK: the North-West diabetes foot care study. Diabetes Care 2005;28:1869–75. Chaturvedi N, Abbott CA, Whalley A, Widdows P, Leggetter SY, Boulton AJ. Risk of diabetes-related amputation in South Asians vs Europeans in the UK. Diabet Med 2002;19:99–104. Chaturvedi N, Stevens LK, Fuller JH, Lee ET, Lu M. Risk factors, ethnic differences and mortality associated with lower-extremity gangrene and
[19]
[20]
[21] [22] [23] [24]
[25]
[26]
[27] [28]
[29] [30] [31]
amputation in diabetes: the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia 2001;44:S65–71. Wolf G, Chen S, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 2005;54:1626–34. David JM, Ole H, Haroldl F. Association between renal failure and foot ulcer or lower extremity amputation in patients with diabetes. Diabetes Care 2008;31 (July (7)):1331–6. Ryan L, Tien YW, Charumathi S. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond) 2015;2:17. Karman MA. Association between high risk foot, retinopathy and HbA1c in Saudi diabetic population. Pak J Physiol 2010;6(2):22–8. Alexiadou Kleopatra, Doupis John. Management of diabetic foot ulcer. Diabetes Ther 2012;3(1):4. Amanda NL, Samuel DJ. The comorbities of diabtes and hypertension: mechanism and approach to target organ protection. J Clin Hypertens 2011;13(April (4)):244–51. Lieza GE, Geert JB, Andrew JK, Elbert SH, Wayne JK, Jerome RM, et al. Risk factor prediction of 10 year dementia in individuals with type 2 diabetes: a cohort study. Lancet Diabetes Endocrinol 2013;1(November (3)):183–90. Anna M, Welli X, Debobra R, Camilla F, Christine W, Enrico B, et al. Cognitive functioning among patients with diabetic foot. J Diabetes Complic 2014;28:863–8. Mohammad Z, Abida M, Jamal A. Diabetic foot ulcer: a review. Am J Intern Med 2015;3(2):28–49. Young H, Knepper B, Hernandez W, Shor A, Bruntz M, Berg C, et al. Psuedomonasaeruginosa; an uncommon cause of diabetic infection. J Am Podiatry Med Assoc 2015;105(March (2)):125–9. El-Tahaway AT. Bacteriology of diabetic foot. Saudi Med J 2000;21(April (4)):244–7. Ramani A, Ramani R, Shivananda PG, Kundaje GN. Bacteriology of diabetic foot ulcers. Indian J Pathol Microbiol 1991;34(April (2)):81–7. Yoga R, Khairul A, Sunita K, Suresh C. Bacteriology of diabetic foot lesions. Med J Malays 2006;61(February (A)):14–6.
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Diabetes & Metabolic Syndrome: Clinical Research & Reviews journal homepage: www.elsevier.com/locate/dsx
Original Article
Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital Ramya Kateela , Alfred J. Augustineb , Shivananda Prabhub , Sheetal Ullalc, Manohar Paib , Prabha Adhikarid,* a
Department of Medicine, Manipal University, Mangalore, India Department of Surgery, Manipal University, Mangalore, India Department of Pharmacology, Manipal University, Mangalore, India d Department of Medicine, Yenepoya University, Deralakatte, Mangalore, India b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 August 2017 Accepted 20 August 2017 Available online xxx
Aim: To evaluate the clinical and microbiological profile of diabetic foot ulcer patients admitted to a tertiary care hospital. Methodology: This study recruited 120 diabetic foot ulcer patients of all grade. Their medical records were evaluated retrospectively. Results: We found that median age of patient was 60(52, 67.75) years. 68.3% of patients were males. Median duration of diabetes mellitus was 15(10, 20) years. Mean HbA1C and fasting glucose was 10.3 2.3 and 167.6 52.42 respectively. Neuropathy (35%) and peripheral vascular disease (23.3%) was major micro vascular and macro vascular complication associated. Different locations of ulcers were toe (23.3%), sole (20%), dorsum (18.3%), shin (16.6%), heel (13.3%), and ankle (8.3%). Bacterial infection was seen in 81.66% patients out of which 23.3% had poly microbial infection. Conclusion: Diabetic foot ulcer patient had poor blood glucose control with elevated HbA1C and fasting blood glucose level. Neuropathy and peripheral vascular disease, hypertension were major complications. Staphylococcus aureus, Pseudomonas aeruginosa were common infecting bacteria. © 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Keywords: Diabetic foot ulcer Complications of diabetes Bacterial infection of foot
1. Introduction The incidence of diabetes mellitus is increasing at an alarming rate along with the complications associated with it. The WHO has estimated that the global prevalence of diabetes has increased from 4.75% in 1980 to 8.5% in 2014 [1]. Diabetes mellitus is associated with several complications. Diabetic foot ulcer is one such complication which has a significant impact on the quality of life of the patient and on the associated health care burden. It is one of the common causes of morbidity, hospital admission and amputation among diabetics. In the clinical population of India, prevalence of diabetic foot ulcer is found to be 3.6% [2]. The approximate lifetime risk of a diabetic patient developing an ulcer is 25% [3,4]. As reported in a south Indian study, patients with diabetes spend 9.3% of their total income towards treatment whereas patients with diabetes and foot ulcer spent 32.3% of their
* Corresponding author. E-mail address: [email protected] (P. Adhikari).
total income towards treatment [5]. Hence diabetic foot ulcer can be considered as an economic and medical threat in health care system. The treatment of diabetic foot ulcer includes multiple approaches. Hence studying about the profile of patients who develop foot ulcers, extent of the disease and the complications associated with it will help health care providers to plan better prevention programs and treatment strategies. Also clinical profile of a disease varies in different geographical area. Hence studying clinical profile of local population will help in better prevention and treatment of a disease. With the above background the present study was undertaken to evaluate the clinical and microbiological profile of diabetic foot ulcer patients. 2. Materials and methods Institutional ethics committee permission was obtained for conduct of the study. Medical records of 120 diabetic patients with foot ulcer were retrieved and reviewed. Patients’ demographic data, associated micro vascular and macro vascular complications,
http://dx.doi.org/10.1016/j.dsx.2017.08.008 1871-4021/© 2017 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
2
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
laboratory values like fasting blood glucose level, glycosylated hemoglobin level, duration of diabetes mellitus, location of ulcer and microbial infection details were noted down. 3. Results Table 1 shows patient’s demographic data, duration diabetes and laboratory values. Graph 1 shows number of patients affected with micro vascular complications like neuropathy, nephropathy and retinopathy. All three micro vascular complication was present in 15%(18) patients. Graph 2 shows the number of patients associated with macro vascular complications like coronary artery disease, cerebrovascular disease and peripheral vascular disease. Hypertension, dementia, dyslipidemia and congestive heart failure were other important complications associated. Table 2 shows the no of patients affected with these complications. Aerobic bacterial infection was seen in 81.66%(98) patients out of which 28.5%(28) patients had poly microbial infection. Table 3 shows different bacteria isolated from diabetic foot ulcer. Graph 3 shows location of ulcer in patient’s foot.
Graph 1. Micro vascular complications associated.
4. Discussion Diabetic foot is one of the most common devastating complications among other chronic complications of diabetes mellitus. It is the leading cause of non traumatic amputation throughout the world [6]. There are multiple factors which lead to development of foot ulcer in diabetic patients which may even result in amputation if not treated. In our study we found that median age of patients was 60(52, 67.75). The proportion of diabetic foot ulcer varied between 1.7 and 3.3% in younger patients and 5 and 10% among older patients, which is similar to previous studies. Old age was considered one of the independent risk factors for the development of diabetic foot ulcer. Risk of ulceration increases two to four fold with age in diabetes [7,8]. Most of the earlier studies have shown a higher rate of diabetic foot among males. Similarly in our study more number of male patients (68%) had diabetic foot ulcer compared to females (32%). This may be because females have less severe neuropathy, increased joint mobility, low foot pressure and better propensity towards self-care compared to men. In addition males are more likely to be exposed to trauma and wear improper foot wear especially in the Indian scenario [9,10]. Another important common risk factor identified for the development of foot ulcer in diabetic patients is longer duration of diabetes mellitus and uncontrolled blood sugar level. In our study median duration of diabetes was 15 years (10, 17) and mean HbA1c and FBS was 10.3 2.3% and 167.6 52.42 mg/dl respectively. Longer the duration of diabetes, more is the micro and macro vascular complications associated with it which in turn
Graph 2. Macro vascular complications associated.
Table 2 Other important complications associated. Complication
Percentage (N)
Hypertension Dyslipidemia Congestive heart failure Dementia
58.3%(70) 15%(12) 11.7%(14) 5%(6)
Table 3 Bacteria Isolated. Bacteria
Percentage (N)
Staphylococcus aureus E. coli Pseudomonas aeruginosa Klebsiella species Proteus species Enterococcus species Streptococcus
40.81%(40) 34.69%(34) 30.61%(30) 12.63%(12) 5.10%(5) 5.10%(5) 1.02%(1)
Table 1 Patients’ demographic and other details. Parameter
Value
Median age (IQR) in years Gender ratio% (n = 120)
60(52,67.75) Male 68% (82) 15(10,17) 10.3 2.3 167.6 52.42 Grade 1 43.3%(52)
Median Duration of diabetes mellitus in years (IQR) Mean HbA1C SD (%) Mean Fasting blood glucose SD(mg/dl) Ulcer grade
Female 32%(38)
Grade 2 46.6%(56)
Grade 3 10%(12)
Grade 4 0
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
Graph 3. Location of ulcer.
results in ulceration of foot and amputation. Studies have shown that patients with a poor glycemic control have a 2–4 fold increased risk of ulceration [7,11]. The most commonly stated microvascular complication which is a risk factor for development of diabetic foot is neuropathy. In our study 35% of patients had neuropathy. Several studies have shown that prevalence of neuropathy in diabetic foot ulcer varies from 8% to 59% [12–15] but it is also reported that Asians have relatively lower diabetic foot complications and amputations compared to Europeans. One of the proposed reason for this is Asians have reduced prevalence of diabetic neuropathy and peripheral artery disease compared to Europeans [16–18]. In our study we found that 25% of diabetic foot ulcer patients had nephropathy. Incidence of diabetic foot ulcer increases with progressive renal impairment. Patients with both diabetes and chronic kidney disease have two to six times risk of getting lower extremity amputation compared to patient with only diabetes. Most studies have claimed atherosclerosisas a common factor and noted an association between peripheral vascular disease and chronic kidney disease [19]. But in our study only 32% of patients who had nephropathy had peripheral vascular disease. These results are similar to those of David J et al. who in their study showed an association between chronic kidney disease and diabetic foot ulcer and lower extremity amputation. This association was present even without clinically apparent peripheral vascular disease. They hypothesized that chronic kidney disease can be used as an early marker for diabetic foot ulcer because hyperglycemia in cells leads to renal damage first, since renal cells are most sensitive and cannot replenish. Skin is affected later which can replenish from neighbouring cells, transient amplifying cells local to the wound and bone marrow–derived cells [20]. Hence we infer that poor glycemic control is the main culprit leading to diabetic nephropathy at first and diabetic foot later. Studies have also found a significant association between diabetic foot ulcer and retinopathy. It can be used as a proxy for severity of diabetes [21]. Decreased vision is one of the risk factors for the development of diabetic foot ulcer. In diabetic retinopathy patient’s decreased vision may lead to trauma and patient may not
3
be able to examine the foot properly [22]. In our study 28.3% patients had retinopathy. Peripheral vascular disease is another commonly stated risk factor for the development of diabetic foot ulcer. In our study 38.5% of patients had peripheral vascular disease. It also increases the risk of lower extremity amputation by delaying healing process. It is also associated with increased incidence of cardiovascular and cerebrovascular events. In our study 26.75% of patients had cardiovascular disease and 3.3% of patients had cerebrovascular events. Hence it is important to diagnose peripheral vascular disease in diabetic patients in order to take early prevention measures to avoid foot ulcer, cardiovascular events and also mortality. In patients with diabetic foot ulcer early recognition and expert assessment are required to determine the need for revascularization to promote ulcer healing [23]. Another important risk factor we observed in our study was hypertension. 58.3% of diabetic foot ulcer patients had hypertension. Studies have shown that approximately 75% of diabetic patients have hypertension. There is a significant amount of overlap between complications of diabetes and hypertension. It is considered one of the risk factors for lower extremity amputation [24]. Previous studies showed that people with diabetes mellitus have a twofold higher risk of developing dementia [25]. Amputation, micro vascular disease and poor glycemic control were associated with impaired cognitive function [26]. But in our study only 4% of patients had dementia. In our study Pseudomonas Sps., Staphylococcus aureus and E. coli were the commonly isolated aerobic bacteria. These results are similar to previous studies [27–31]. 5. Conclusion In our study we noted that diabetic foot ulcer patients had prolonged duration of diabetes with poor blood glucose control. Along with neuropathy and peripheral vascular disease hypertension, nephropathy, retinopathy and coronary artery disease were major complications associated. Most of the wounds were infected with Pseudomonas sps., Staphylococcus aureus and E. coli. Hence treating diabetic foot ulcer requires a multidisciplinary team consisting of a podiatrist, dialectologist, a vascular surgeon, infectious disease specialist, neurologist in order to address all the complications associated, so that incidence of lower extremity amputation reduces. Conflicts of interest Authors declare no conflict on interest. References [1] http://www.who.int/mediacentre/factsheets/fs312/en/. (Accessed 3 March 2017). [2] Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcer in patients with diabetes. JAMA 2005;293:217–28. [3] International Working Group on the Diabetic Foot. Epidemiology of Diabetic Foot Infections in a Population Based Cohort. Noordwijkerhout, the Netherlands: International Working Group on the Diabetic Foot; 2003. [4] Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJM. Diabetic foot syndrome: evaluating the prevalence and incidence of foot pathology in Mexican Americans and non-Hispanic whites from a diabetes disease management cohort. Diabetes Care 2003;26:1435–8. [5] Shobhana R, Rama Rao P, Lavanya A, Vijay V, Ramachandran A. Cost burden to Diabetic patients with foot complications- a study from Southern India. JAPI 2000;48:12. [6] Frykberg RG, Armstrong DG, Giurini J, Edwards A, Kravette M, Kravitz S, et al. Diabetic foot disorders: a clinical practice guideline. American College of Foot and Ankle Surgeons. J Foot Ankle Surg 2000;39(S5):S1–S60. [7] Reiber GE, Ledoux WR. Epidemiology of Diabetic Foot Ulcers and Amputations: Evidence for Prevention the Evidence Base for Diabetes Care. John Wiley &
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008
G Model DSX 854 No. of Pages 4
4
R. Kateel et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2017) xxx–xxx
[8]
[9] [10] [11]
[12]
[13]
[14]
[15] [16]
[17]
[18]
Sons, Ltd; 2003. p. 641–65. . Available: http://dx.doi.org/10.1002/0470846585. ch28. Khalid AR, Mohammad AD, Samir O, Amira MY, Shazia NS, Heba MI, et al. Diabetic foot complications and their risk factors from large retrospective cohort study. PLoS One 2015;10(5):e0124446. Monica E. Gender difference in diabetes-related lower extremity amputations. Clin Orthop Relat Res 2011;469(July (7)):1951–5. Dinh T, Veves A. The influence of gender as a risk factor in diabetic foot ulceration. Wounds 2008;20(May (5)):127–31. Jyothilekshmy V, Arun SM, Abraham Suja. Epidemiology of diabetic foot complications in podiatry clinic of a tertiary hospital in south India. Indian J Health Sci 2015;8(1):48–51. Young MJ, Boulton AJ, MacLeod AF, Williams DR, Sonksen PH. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993;36:150–4. Partanen J, Niskanen L, Lehtinen J, Mervaala E, Siitonen O, Uusitupa M. Natural history of peripheral neuropathy in patients with non-insulin-dependent diabetes mellitus. N Engl J Med 1995;333:89–94. Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology 199343: 817–817. Deli G, Bosnyak E, Pusch G, Komoly S, Feher G. Diabetic neuropathies: diagnosis and management. Neuroendocrinology 2013;98:267–80. Abbott CA, Garrow AP, Carrington AL, Morris J, Van Ross ER, Boulton AJ, et al. Foot ulcer risk is lower in South-Asian and African-Caribbean compared with European diabetic patients in the UK: the North-West diabetes foot care study. Diabetes Care 2005;28:1869–75. Chaturvedi N, Abbott CA, Whalley A, Widdows P, Leggetter SY, Boulton AJ. Risk of diabetes-related amputation in South Asians vs Europeans in the UK. Diabet Med 2002;19:99–104. Chaturvedi N, Stevens LK, Fuller JH, Lee ET, Lu M. Risk factors, ethnic differences and mortality associated with lower-extremity gangrene and
[19]
[20]
[21] [22] [23] [24]
[25]
[26]
[27] [28]
[29] [30] [31]
amputation in diabetes: the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia 2001;44:S65–71. Wolf G, Chen S, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 2005;54:1626–34. David JM, Ole H, Haroldl F. Association between renal failure and foot ulcer or lower extremity amputation in patients with diabetes. Diabetes Care 2008;31 (July (7)):1331–6. Ryan L, Tien YW, Charumathi S. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond) 2015;2:17. Karman MA. Association between high risk foot, retinopathy and HbA1c in Saudi diabetic population. Pak J Physiol 2010;6(2):22–8. Alexiadou Kleopatra, Doupis John. Management of diabetic foot ulcer. Diabetes Ther 2012;3(1):4. Amanda NL, Samuel DJ. The comorbities of diabtes and hypertension: mechanism and approach to target organ protection. J Clin Hypertens 2011;13(April (4)):244–51. Lieza GE, Geert JB, Andrew JK, Elbert SH, Wayne JK, Jerome RM, et al. Risk factor prediction of 10 year dementia in individuals with type 2 diabetes: a cohort study. Lancet Diabetes Endocrinol 2013;1(November (3)):183–90. Anna M, Welli X, Debobra R, Camilla F, Christine W, Enrico B, et al. Cognitive functioning among patients with diabetic foot. J Diabetes Complic 2014;28:863–8. Mohammad Z, Abida M, Jamal A. Diabetic foot ulcer: a review. Am J Intern Med 2015;3(2):28–49. Young H, Knepper B, Hernandez W, Shor A, Bruntz M, Berg C, et al. Psuedomonasaeruginosa; an uncommon cause of diabetic infection. J Am Podiatry Med Assoc 2015;105(March (2)):125–9. El-Tahaway AT. Bacteriology of diabetic foot. Saudi Med J 2000;21(April (4)):244–7. Ramani A, Ramani R, Shivananda PG, Kundaje GN. Bacteriology of diabetic foot ulcers. Indian J Pathol Microbiol 1991;34(April (2)):81–7. Yoga R, Khairul A, Sunita K, Suresh C. Bacteriology of diabetic foot lesions. Med J Malays 2006;61(February (A)):14–6.
Please cite this article in press as: R. Kateel, et al., Clinical and microbiological profile of diabetic foot ulcer patients in a tertiary care hospital, Diab Met Syndr: Clin Res Rev (2017), http://dx.doi.org/10.1016/j.dsx.2017.08.008