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European Journal of Applied Sciences – Vol. 11, No. 5

Publication Date: October 25, 2023

DOI:10.14738/aivp.115.15698

Ousmane, F., Goïta, Y., Koné, A., Mariko, M., Traore, B., Dramé, S. I., Doumbia, N., Fomba, M., Bissan, A. T., Dabo, A., Diallo, M.,

Bamba, O., Koné, A., Karambiry, M. Koné, H., Kouriba, B., & Traoré, A. (2023). Clinico-Biological Aspects of Undernutrition in

Diabetic Patients Hospitalized in The Medical Department of The Mali Hospital. European Journal of Applied Sciences, Vol - 11(5).

431-442.

Services for Science and Education – United Kingdom

Clinico-Biological Aspects of Undernutrition in Diabetic Patients

Hospitalized in The Medical Department of The Mali Hospital

Faridatou Ousmane

Faculty of Pharmacy, University of Sciences, Techniques and Technologies

of Bamako, Mali

Yaya Goïta

Faculty of Pharmacy, University of Sciences, Techniques and Technologies

of Bamako, Mali, and medical biology and anatomopathology laboratory

department Diagnosis of Covid-19, University Hospital Center Mali

Hospital, Bamako, Mali

Amadou Koné

Department of Medicine, and Endocrinology, University Hospital Center

Mali Hospital, Bamako, Mali and National Center for Scientific and

Technological Research (CNRST) and Faculty of Medicine and Dentiste,

University of Sciences, Techniques and Technologies of Bamako, Mali

Modibo Mariko

Department of Medicine, and Endocrinology, University Hospital Center

Mali Hospital, Bamako, Mali and Faculty of Medicine and Dentiste,

University of Sciences, Techniques and Technologies of Bamako, Mali

Bah Traore

Department of Medicine, and Endocrinology, University Hospital Center

Mali Hospital, Bamako, Mali

Sidiki Ibrahim Dramé

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali and

Faculty of Medicine and Dentiste, University of Sciences, Techniques and

Technologies of Bamako, Mali

Nanko Doumbia

Department of Medicine, and Endocrinology, University Hospital Center

Mali Hospital, Bamako, Mali and National Center for Scientific and

Technological Research (CNRST)

Minkoro Fomba

National Center for Scientific and Technological Research (CNRST)

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European Journal of Applied Sciences (EJAS) Vol. 11, Issue 5, October-2023

Aboubacar Tiétié Bissan

Faculty of Pharmacy, University of Sciences, Techniques and Technologies

of Bamako, Mali

Abdoulaye Dabo

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Mamadou Diallo

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Oussamatou Bamba

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Adama Koné

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Moussa Karambiry

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Halidou Koné

Medical biology and anatomopathology laboratory department Diagnosis

of Covid-19, University Hospital Center Mali Hospital, Bamako, Mali

Bourèma Kouriba

Faculty of Pharmacy, University of Sciences, Techniques and Technologies

of Bamako, Mali

Assa Traoré

Faculty of Medicine and Dentiste, University of Sciences, Techniques and

Technologies of Bamako, Mali

ABSTRACT

Introduction: Undernutrition is a frequent and often unrecognized pathology in the

hospital environment. Its consequences are significant both medically and

financially, as it increases hospital length of stay, morbidity and mortality. The aim

of this study was to assess the clinical and biological aspects of undernutrition in

diabetic patients hospitalized in the medical department of the Mali Hospital.

Methodology: A survey was carried out on 65 diabetic patients admitted to hospital

between April 5, 2022 and November 4, 2022. The diagnosis of undernutrition was

based on the 2021 Haute Autorité de Santé (HAS) diagnostic criteria, and the

severity of undernutrition was assessed using the International Obesity Tast Force

(IOTF) curves in children (<18 years) and albumin measurement in adult diabetic

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Ousmane, F., Goïta, Y., Koné, A., Mariko, M., Traore, B., Dramé, S. I., Doumbia, N., Fomba, M., Bissan, A. T., Dabo, A., Diallo, M., Bamba, O., Koné,

A., Karambiry, M. Koné, H., Kouriba, B., & Traoré, A. (2023). Clinico-Biological Aspects of Undernutrition in Diabetic Patients Hospitalized in The

Medical Department of The Mali Hospital. European Journal of Applied Sciences, Vol - 11(5). 431-442.

URL: http://dx.doi.org/10.14738/aivp.115.15698

patients (18 years and over). The survey method consisted in collecting information

on the clinical and biological aspects of undernourished diabetic patients. Results:

This Study showed that the age of our patients ranged from 7 to 82 years, with an

average age of 50.96 ± 22.44 years. Females predominated over males, with 52%

and 48% respectively. Type 2 diabetes predominated, with a frequency of 75%

versus 25% for type 1 diabetes. The mean albumin level was 26.81 ± 5.53 g/l, with

moderate to severe undernutrition at 33.96% and 64.15% respectively. Severe

undernutrition was 83%, compared with 17% of moderate undernutrition in

diabetic children, according to International Obesity Tast Force (IOTF) curves. The

mean BMI was 19.57 ± 4.39 kg/m2. From this study, we could conclude that the

decrease in albumin levels was correlated with the high frequency of

undernutrition in diabetic patients. It would be interesting to assess the nutritional

status of diabetic patients on admission, in order to avoid the morbidity and

mortality associated with undernutrition.

Keywords: undernutrition, diabetes, serum albumin, Mali.

INTRODUCTION

Undernutrition is a pathological condition resulting from insufficient protein-energy intake to

cover the body's metabolic needs (1). In hospitalized patients, it affects almost one in two

patients on admission, and its management remains inadequate despite recent progress (2). Its

prevalence is between 30% and 50% among patients admitted to hospital (2). A NHANES study

reports a higher prevalence of over 20% of undernutrition in diabetics, or over 30% risk of

undernutrition (3), leading to muscular weakening, altered general condition, delayed wound

healing, reduced immunological performance and diminished capacity to adapt and resist

aggression (4). In diabetics, this phenomenon is of particular concern, as it can lead to a

worsening of the complications associated with the disease. Indeed, diabetes is a metabolic

disorder characterized by chronic hyperglycemia resulting from a defect in insulin secretion

and/or action (5). Glycemic imbalance has been shown to lead to protein undernutrition. This

is partly explained by a reduction in insulin availability and/or action, due to insulin resistance

in skeletal muscle (6). This undernutrition associated with diabetes is thought to have a major

impact on bone metabolism, muscle function and immune function (7). If not treated early, the

affected person will be drawn into a downward spiral that could lead to death (7). For many

years, undernutrition was regarded as an ancillary medical problem. Indeed, for most nursing

staff, a hospitalized patient was only admitted for his or her main pathology; all other

treatments were only minor. As a result, undernutrition was all too often relegated to the

background (8). As a result, many emerging countries are ignoring this major public health

problem (9,10). In Western countries, the considerable additional costs associated with

undernutrition (11) should lead healthcare professionals in emerging countries to take this

problem seriously.

In Mali, no study has been reported on the prevalence of undernutrition in diabetic subjects.

This led us to conduct this study, the aim of which was to evaluate the clinico-biological aspects

of undernutrition in diabetic patients hospitalized in the medical department of the Mali

hospital.

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European Journal of Applied Sciences (EJAS) Vol. 11, Issue 5, October-2023

MATERIALS AND METHODS

Ethical aspects: the study was conducted in accordance with the ethical standards set out in the

Declaration of Helsinki (1983). Inclusion in the study was carried out in accordance with the

rules of the legislation in force at the hospital in Mali, and with strict respect for the

confidentiality of patients' identities and the results of their analysis.

Type of Study and Participants

This was a prospective, analytical study carried out in the Medicine and Medical Biology and

Anatomopathology Laboratory departments of Mali Hospital. The study included 65 diabetic

patients hospitalized in the Medicine Department of Mali Hospital from April to November

2022. Eligible patients were selected according to the following inclusion criteria:

Undernourished diabetic patients hospitalized in the Mali Hospital Medicine Department,

regardless of type of diabetes, sex or age.

Sample Collection and Parameters Studied

A survey form specially designed for this study enabled us to collect information on the

sociodemographic, clinical and biological aspects of undernutrition in diabetic patients. The

form comprises a series of questionnaires completed by undernourished diabetic patients. We

recorded age, sex and clinical aspects of undernutrition, namely anorexia, apathy, physical

asthenia, weight loss and body mass index (BMI).

Albumin levels (35-54 g/L) were measured in patients aged 18 and over to determine the

degree of undernutrition. Creatinine levels (male: 70-115 μmol, female: 44-80 μmol/L) and

creatinine clearance (80-120 ml/min) calculated by the CKD-EPI formula were determined to

assess renal function. HbA1c (3.5-6%) was measured to assess glycemic control. And finally, C- reactive protein (0 - 6 mg/L) was measured to determine whether there was an inverse

correlation between albumin and CRP.

Blood samples were taken from hospitalized patients who had been in a young state from 8 a.m.

to 12 noon. Blood samples collected in heparin tubes for albumin, creatinine, blood glucose and

CRP analysis were centrifuged at +4°C for 10 minutes at 3500 rpm/min. The EDTA tube

specimen was used for blood count and HbA1c analysis.

International Obesity Tast Force (IOTF) curves in diabetic children (<18 yrs) were used to

determine undernourished cases and the degree of undernutrition in them. The diagnosis of

undernutrition was based on the 2021 Haute Autorité de Santé (HAS) diagnostic criteria.

Analytical Procedure

The Mindray BS-480 analyzer was used for albumin determination. The colorimetric method,

also known as the Bromocresol Green (BCG) dye method, was used for albumin determination.

BCG added to plasma produces a bluish-green color that absorbs light at a wavelength of 605

nm. The amount of light absorbed is proportional to the concentration of albumin in the plasma.

The Pentra C400 analyzer was used to measure blood glucose, creatinine and C-reactive

protein. The glucose oxidase enzymatic method was used to measure blood glucose levels.

Glucose oxidase catalyzes the transformation of glucose into gluconic acid and hydrogen

peroxide (H202). The colorimetric indicator is quinoneimine, which is generated from 4-

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Ousmane, F., Goïta, Y., Koné, A., Mariko, M., Traore, B., Dramé, S. I., Doumbia, N., Fomba, M., Bissan, A. T., Dabo, A., Diallo, M., Bamba, O., Koné,

A., Karambiry, M. Koné, H., Kouriba, B., & Traoré, A. (2023). Clinico-Biological Aspects of Undernutrition in Diabetic Patients Hospitalized in The

Medical Department of The Mali Hospital. European Journal of Applied Sciences, Vol - 11(5). 431-442.

URL: http://dx.doi.org/10.14738/aivp.115.15698

aminoantipyrine (4-AAP) and sodium P-hydroxybenzoic acid by hydrogen peroxide under the

catalytic action of peroxidase (Trinder reaction). The intensity of the coloration measured on a

spectrophotometer is proportional to the glucose concentration.

Creatinine levels were measured using the colorimetric Trinder enzymatic method. The

enzymes creatinase and sarcosidase hydrolyze endogenous creatine, which is converted to

peroxide and then eliminated by catalase. Catalase is inhibited by sodium azide, and

creatininase and 4-Amino-antipyrine (4-AA) are added. Thus, only creatine generated from

creatininase is sequentially hydrolyzed by creatinase and sarcosine oxidase to produce

hydrogen peroxide. This hydrogen peroxide is measured by coupling with a peroxide- catalyzing reaction, which forms a colored complex with N-ethyl-n-sulphopropyl-mtoluidine

(TOPS)/4-AA.

The immunoturbidimetric method was used to measure CRP. It involves measuring the amount

of specific protein in a biological sample by detecting the variation in turbidity caused by the

reaction between the specific antibody and the target antigen. In the case of CRP, the analyzer

uses a reagent containing anti-CRP antibodies and latex particles. When the CRP-containing

sample is added to the reagent, the antibodies bind to the CRP, forming aggregates which

increase the turbidity of the solution. The amount of CRP is then measured as a function of the

change in turbidity.

The Mindray H50P analyzer was used to measure glycated hemoglobin A1 (HbA1c). High- performance liquid chromatography (HPLC) was the principle of the assay method. HPLC uses

a chromatography column to separate the different haemoglobin fractions present in the

sample, including HbA1c.Once the different fractions have been separated, HbA1c is detected

and quantified using a specific detector. The amount of HbA1c present in the sample is

expressed as a percentage of total hemoglobin.

Univariate Statistical Analysis

The chi2 statistical test and the Fisher's exact test according to numbers were used to compare

categorical variables. The Anova test was used to compare means. Differences were considered

significant if the probability (p) was p ≤ 0.05.

RESULTS

In this study, 52% of cases were predominantly female, compared with 48% male. The sex ratio

was 0.91. Denutrated diabetic patients admitted to the medical ward were divided into age

groups according to the HAS 2021 diagnostic criteria. Patients aged between 18 and 69

accounted for 60% of cases, followed by those aged 70 and over (21.54%). The under-18 age

group accounted for 18.48%. The mean age of included patients was 50.96 ± 22.44 years, with

a minimum of 7 years and a maximum of 82 years. For a total of 65 patients, type 2 diabetes

accounted for 75% (n=49) versus 25% (n=16) of type 1 diabetes. With regard to the etiologies

of undernutrition in diabetic patients, infection ranked highest, with a rate of 87.69%. Among

diabetic complications, foot wounds accounted for 55.38% of causes of undernutrition.

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European Journal of Applied Sciences (EJAS) Vol. 11, Issue 5, October-2023

Table I: Distribution of undernourished diabetic patients according to clinical signs of

undernutrition

Clinical signs Workforce(N=65) Frequency

Emaciation 59/65 90,77%

Physical Asthenia 52/65 80%

Anorexia 49/65 75,38%

Apathy 35/65 53,85%

The clinical signs of undernutrition were weight loss in 90.77% of cases, followed by physical

asthenia (80%), anorexia (75.38%) and apathy (53.85%).

Table II: Distribution of malnourished diabetic patients by body mass index (BMI)

BMI Number of staff (Average ± standard deviation) Frequency

Underweight 27 (15.59 ± 2.25 kg/m2

) 42,62%

Normal 25 (21.16 ± 1.86 kg/m2

) 37,25%

Overweight 10 (26.32 ± 1.38 kg/m2

) 15,1%

Not determined 3 4,53%

Total 65 100%

The mean BMI was 19.57 ± 4.39 kg/m2, with extremes of 10.81 kg/m2 and 28.51 kg/m2. Most

of the undernourished diabetic patients in this study were underweight (42.62%), with a mean

of 15.59 ± 2.25 kg/m2. Overweight was estimated at 15.1%, with a mean of 26.32 ± 1.38 kg/m2.

BMI was not determined in 4.53% of stroke patients, due to a lack of materials for weight

measurement in bedridden patients. Assessment of the severity of undernutrition using the

International Obesity Tast Force (IOTF) curves in children (<18 years) showed that most

undernourished diabetic children were severely undernourished (83%), compared with 17%

with moderate undernutrition.

Figure 1: Distribution of undernourished diabetic children according to severity of

undernutrition using the International Obesity Tast Force (IOTF) curves for children.

0

2

4

6

8

10

12

14

N=12

<17IOTF <18,5IOTF

Severe

undernutrition

N=10 (83%)

Moderate

undernutrition

N=2 (17%)

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Ousmane, F., Goïta, Y., Koné, A., Mariko, M., Traore, B., Dramé, S. I., Doumbia, N., Fomba, M., Bissan, A. T., Dabo, A., Diallo, M., Bamba, O., Koné,

A., Karambiry, M. Koné, H., Kouriba, B., & Traoré, A. (2023). Clinico-Biological Aspects of Undernutrition in Diabetic Patients Hospitalized in The

Medical Department of The Mali Hospital. European Journal of Applied Sciences, Vol - 11(5). 431-442.

URL: http://dx.doi.org/10.14738/aivp.115.15698

A reduction in food intake ≥ 50% for more than a week compared with usual food intake was

observed in 83% of our patients. Patients who maintained usual food intake accounted for 17%.

Figure 2: Distribution of malnourished diabetic patients according to food bolus reduction.

Table III: Biological characteristics of undernutrition in diabetic patients.

Parameters Averages ± Standard deviations

[Minimum-Maximum]

Reference values

Albuminemia (g/l) 26.81 ± 5.53

[11.50-38.10]

35.20-52.30 g/L

CRP (mg/l) 68.68 ± 65.30

[0,01-218]

< 6 mg/L

Creatinine (μmol/l) 66.12 ± 46.01

[9,72-326,9]

-Male: 71-115μmol/L

-Female: 53-106μmol/L

Clearance (ml/min) 133.12 ± 76.04

[14-524,79]

80-120 ml/min

Blood glucose (g/l) 2.96 ± 1.58

[0.30-7.6]

< 1.26 g/L

HbA1c (%) 10.22 ± 3.62

[3,2-16,95]

3,5-6%

Haemoglobin level (g/dl) 9.10 ± 2.42 g/dL

[3,50-13]

12-16 g/dL

For the biological characteristics of undernutrition in diabetics, we obtained: a mean albumin

level of 26.81 ± 5.53 g/L. The mean CRP was 68.68 ± 65.30 mg/L. The mean creatinine level

was 66.12 ± 46.01 μmol/L, with a mean clearance of 133.12 ± 76.04 ml/min. Carbohydrate

homeostasis was unbalanced, with a mean HbA1c level of 10.22 ± 3.62% and a mean blood

glucose level of 2.96 ± 1.58. Mean hemoglobin was 9.10 ± 2.42 g/dL.

NO

(N=11)

17%

YES

(N=54)

83%

N=65

NO YES

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Ousmane, F., Goïta, Y., Koné, A., Mariko, M., Traore, B., Dramé, S. I., Doumbia, N., Fomba, M., Bissan, A. T., Dabo, A., Diallo, M., Bamba, O., Koné,

A., Karambiry, M. Koné, H., Kouriba, B., & Traoré, A. (2023). Clinico-Biological Aspects of Undernutrition in Diabetic Patients Hospitalized in The

Medical Department of The Mali Hospital. European Journal of Applied Sciences, Vol - 11(5). 431-442.

URL: http://dx.doi.org/10.14738/aivp.115.15698

Table VII: Relationship between CRP levels and foot wounds.

There was a statistically significant association between CRP levels and foot wounds.

DISCUSSION

We conducted a prospective, cross-sectional study in the Department of Medicine in

collaboration with the biomedical and anatomopathology laboratory of Mali Hospital. The

study concerned diabetic patients of all types, sex and age, and focused on undernutrition. A

total of 65 diabetic patients were recruited, representing a hospital frequency of 39.39%.

Females represented 52% of our sample, with a sex ratio of 0.91. The presence of more risk

factors for undernutrition in the female sex could explain this female predominance. This

female predominance was also obtained by Mahjoub et al, (12) and Omri et al, (13) with 53%

and 56% respectively. The fact that the average age of women is higher than that of men, at

53.29 ± 25.64 years and 48.41 ± 23.70 years respectively, could partly explain why women are

more likely than men to suffer from protein-energy undernutrition. Disturbances in the

regulation of protein metabolism, a poor metabolic response to diet, are linked to a lack of

qualitative and quantitative protein intake in the elderly, and to insulin resistance in peripheral

tissues (14). The balance between protein synthesis and degradation processes determines the

evolution of protein mass, which in turn depends on lean body mass (15).

Our study reported an average age of 50.96 ± 22.44 years. According to the literature, advanced

age accompanied by from a significant increase in the frequency of undernutrition, particularly

protein-energy undernutrition due to reduced dietary intake, caused by physiological changes

and increased needs during pathologies (more frequent in this aging terrain) insufficiently

compensated by intakes (16) could explain this average age of fifty years. This result differs

from that of Omri et al. who found an average age of 71.09 ± 5.19 years (13). This difference in

mean age may be explained by the fact that their study was based on the evaluation of

undernutrition in elderly diabetic subjects (65 years and over), whereas ours included all

diabetic patients, regardless of age and type of diabetes.

The nosological type of diabetes found was type 2 in 75% of cases, followed by type 1 in 25%.

This could be explained by the fact that, according to the IDF, type 2 diabetes remains and

continues to be frequent, manifesting itself most often with ageing and also increasingly in

younger adults in view of their sedentary lifestyle. A preference for sugary foods, overweight

(17), lifestyle changes and the westernization of our cultures have been cited in several

publications as factors in the onset of metabolic and cardiovascular diseases (18,19).

In our series of determinations of biological parameters, carbohydrate homeostasis was

unbalanced in 63.28% of our patients, with a mean HbA1c level of 10.22 ± 3.62%. This result is

Diabetic foot

CRP rate No Yes Total

0-10 mg/l 10(34,48%) 4(11,11%) 14(21,54%)

11-49 mg/l 12(41,38%) 6(16,67%) 18(27,69%)

50-327 mg/l 7(24,14%) 26(72,22%) 33(50,77%)

Total 29(100%) 36(100%) 65(100%)

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comparable with those of Omri et al, (13) and Mizouri et al, (20) who found mean glycated

haemoglobin A1 levels of 10.25 ± 1.8% and 10.2% respectively. This glycaemic imbalance could

be explained by the presence of hypercatabolism, during which pro-inflammatory cytokines

stimulate the secretion of TSH, glucagon and cortisol, thereby reducing insulin secretion (21).

Also, in these malnourished subjects, the onset of an inflammatory syndrome could lead to

stress-related hyperglycaemia (22).

The mean body mass index was 19.57 ± 4.39 kg/m2 in the population studied. This normal

average BMI in no way excludes an underlying state of undernutrition. This is also probably

why undernutrition in a subject with a normal BMI is easily overlooked, even in the context of

a chronic disease such as diabetes (23). Changes in body composition are the most striking

evidence of this paradox, since the reduction in muscle mass and the increase in fat mass are

not always accompanied by a marked reduction in body weight, hence the difficulty in defining

this protein-energy loss in obese, overweight or normal-weight subjects (23). In spite of this

paradox, we found in the diabetic patients included a combination of exogenous and

endogenous undernutrition by reduction of the food bolus (83%) due to anorexia (75.38%) and

by hypercatabolism due to infections (87.69%) could explain this decrease in albumin levels

with 26.81 ± 5.53 g/l in the study population. In fact, the body responds to any severe

aggression with a hypercatabolism syndrome resulting in an over production of

proinflammatory cytokines which stimulate the cells defending against the aggression and

modify the metabolism to supply these cells with nutrients which, in the absence of sufficient

food intake, are drawn from the body's nutritional reserves. This is associated with a change in

hepatic synthesis of proteins in the acute phase of inflammation, which are necessary for the

defence and healing processes (24).

We reported no significant difference between CRP and albumin (P=0.2731). The mean CRP

obtained in this study was 68.68 ± 65.30 mg/l. This result is not comparable with that of Veyrie

et al (25), who found mean albumin and CRP levels of 24 ± 3 g/l and 108 ± 86 mg/l respectively.

This increase in CRP could be linked to the high frequency of infections found in 87.69% of our

patients, with a statistically significant difference P = 0.0001. Compared with the study by

Veyrie et al (25), which only included diabetic patients with a foot sore, our study included

diabetic patients with or without a foot sore, with a statistically significant difference of P =

0.0006 between CRP and diabetic foot. This inflammation correlated with an increase in CRP

and a decrease in albumin in patients with a foot wound has been reported in the literature

(26), explaining a change in CRP concentration according to the type of wound grade in

diabetics.

CONCLUSION

The diabetic population is at increased risk of undernutrition because of the impact of this

disease on metabolism and glycaemia regulation. We observed a significant association

between clinical and biological nutritional parameters, in particular albumin, and the

occurrence of an inflammatory syndrome. Our study showed that the frequency of hospital

undernutrition is high in diabetic subjects. Overall, this study highlights the importance of

regularly assessing the nutritional status of hospitalized diabetic patients, given the

complications that undernutrition can cause.

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Clin Metabolism. 2005 Sep 1;19(3):138–42.

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1;43(2):67-71.

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