Podiatry risk in diabetic pilgrims: a prospective study in Tunisia

Introduction

The Hajj pilgrimage is one of the five pillars of Islam. Every practicing Muslim is bound by faith to do it at least once in his life if he is physically and financially capable. During the journey to Mecca for Hajj, pilgrims perform a series of religious rituals, including barefoot circuits around the holy mosque - Tawaf - and walk between two hills, Safa and Marwah, for long hours. They are also required to spend five days in tents in the Mina Valley where sanitation is very basic, in a hot climate, where the average temperatures can reach 45 °C in the summer.¹

The global prevalence of diabetes mellitus is estimated at 10.5% and this prevalence increases with age.² Given that approximately 2 million Muslims perform the pilgrimage each year, many of them are aged 60 and above, it was projected that the number of pilgrims with diabetes could surpass 340,000 annually.^3,4

Diabetes mellitus is characterized by various complications, including retinopathy, neuropathy, nephropathy, and an increased risk of cardiovascular diseases. Diabetes complications affecting the lower limbs are common, complex, and costly.⁵ People with diabetes are exposed to a range of complications during the pilgrimage, with diabetic foot reported once to be one of the most common causes of admissions in two pilgrimage site hospitals.⁶ However, few studies have studied the podiatry risk in pilgrims with diabetes. The purpose of this study was to evaluate the risk of foot lesions in diabetic pilgrims and to assess the degree of knowledge of diabetic subjects regarding podiatric risk.

Methods

Study variables and data collection

The evaluation was made before and after the pilgrimage. It was based on an anamnesis, a general somatic examination, and a foot examination. The evaluation of peripheral neuropathy was made using the Semmes-Weinstein 10g monofilament test and the DN4 score.

Peripheral arteriopathy was assessed by calculating the arm-ankle index using a pocket Doppler ultrasound machine. A blood test was also requested, including fasting blood sugar, glycated hemoglobin (A1C), renal and lipid blood tests. The grade of podiatric risk was specified for each patient, based on the classification of “The International Working Group on The Diabetic Foot (IWGDF)”.⁷

Knowledge of diabetic foot risks and its preventive measures were evaluated through a survey consisting of 16 questions. Each question was noted 1 if the answer was “Yes”, and 0 if the answer was “No”. A score from 0 to 16 was then determined for each patient which helped to avoid information biases (Figure 1).

Figure 1. Knowledge and preventive measures score for diabetic foot.

Results

Evaluation of diabetic foot education level

Only 20.9% of patients reported that they had received at least one podiatry risk education session from their attending physician. When assessing practical knowledge, the average level of knowledge was 8.3±3.4 out of 16 (Figure 2).

Figure 2. Boxplot of the knowledge and preventive measures score for diabetic foot.

Clinical examination of diabetic feet after the pilgrimage

The evaluation after the pilgrimage concerned 31 patients. The remaining 12 patients were lost to follow-up. The clinical exam showed that hyperkeratosis was the most common form of podiatric lesions (96.8%) as well as fungal infections of the nails and inter-toe spaces (61.3%).

The occurrence of superficial fungal infection of the foot was significantly correlated with the history of inter-toe fungal infection or onychomycosis (p=0.03). However, it wasn’t correlated with glycemic control or with anti-diabetic treatment.

Three patients had foot ulcers which were mainly due to walking injuries and unsuitable shoes (Figure 3). Hospitalization was indicated in only one case of foot ulcer with infection signs, but he refused so that he could perform the rituals and he was given oral antibiotics.

Figure 3. Podiatric lesions in three diabetic patients during the pilgrimage.

Note: Patient 1 (A) presented an ulceration in the big toe (purple arrow), second toe (green arrow), and next to the first metatarsal (orange arrow). Patient 2 (B) had dry gangrene in the second toe. Foot ulcer before (C) and after (D) debridement in patient 3.

The study of the risk of developing a foot ulcer showed that it was significantly associated with lower total cholesterol, HDL cholesterol, and LDL cholesterol and a higher triglyceride level (p respectively 0.02, 0.02, 0.01, and 0.04) (Table 4).

Table 4. Assessment of risk factors for the occurrence of a foot ulcer in Tunisian diabetic patients during pilgrimage.

Characteristics	Foot ulcer
	Yes	No	p
Age (years)	63.6±4.9	62.5±4.8	0.63a
Length of diabetes (years)	20.0±6.5	12.1±9.4	0.14a
Tobacco	50%	16.6%	0.42b
Body mass index (kg/m2)	30.9±5.9	28.9±4.2	0.89a
Glycated hemoglobin (%)	9.2±2.5	7.7±1.2	0.29a
Cholesterol (mmol/L)	2.8±0.2	4.4±1	0.02*a
Triglycerides (mmol/L)	2.0±0.5	1.3±0.7	0.04*a
HDL-cholesterol (g/L)	0.3±0.1	0.4±0.1	0.02*a
LDL-cholesterol (g/L)	0.4±0.1	0.9±0.3	0.01*a

a Analyzed using Mann-Whitney U test.

b Analyzed using χ²-Test (2-sided).

* Statistically significant at p=0.05.

Furthermore, the risk of developing a foot ulcer was not correlated with age, tobacco, or body mass index (Table 4). The study of other risk factors linked to diabetes (length of diabetes, insulin treatment, A1C, existence of neuropathy or ischemia, grade of podiatric risk, and level of knowledge) did not show significant correlations.

A binary logistic regression was performed to define independent predictors of the occurrence of a foot ulcer (variables with p < 0.2 were included). In multivariate analysis, no factor was significantly correlated to a higher risk of foot ulcer.

However, there was a significant increase in the systolic pressure index in the left as well as the right foot after the pilgrimage (1.03±0.19 vs 1.11±0.19 and 1.03±0.28 vs 1.11±0.18, p <0.05).

Discussion

During the Hajj pilgrimage, Muslims are required to perform physically strenuous rituals in crowded and hot environments, which can present significant challenges, especially for individuals with pre-existing health conditions such as diabetes mellitus. The combination of these factors increases the risk of foot lesions, particularly among those with diabetic neuropathy.⁸

Foot injuries represented an important part of the reasons for admissions among diabetic patients.⁹ A study carried out in tertiary care facilities in Saudi Arabia, to assess the causes of admissions, showed that 31.9% of a total 689 emergency patients had diabetes.¹⁰ In our study, hospitalization was indicated in only one case.

Diabetic foot ulcers are commonly caused by repetitive stress on areas that are susceptible to strong vertical or shear stress in patients with diabetic neuropathy. The addition of peripheral arterial disease further contributes to the development of foot ulcers.¹¹ Our study revealed that ischemia and neuropathy were present in 30.2% and 18.6% of patients, respectively. Plantar hyperkeratosis was observed in 88.1% of the population. These findings underscore the importance of addressing both neuropathy and arterial disease in the prevention and treatment of diabetic foot ulcers.

It has been demonstrated that education on the autonomous management of diabetes and its complications is effective in achieving therapeutic goals. Patients who have not received this education are four times more likely to develop complications compared to those who have.¹² Moreover, educational interventions can reduce the risk of amputation by up to 85% and decrease the associated cost of care.¹³

Only 20.9% of our patients have received therapeutic education regarding podiatric risks. This percentage varied greatly between countries. In developed countries, most patients receive information and practical advice for preventing diabetic foot complications, with rates as high as 71.3% in the United Kingdom.¹⁴ In developing countries, the therapeutic education rate was lower, with only 48% of patients in Tanzania for example.¹⁵

This lack of education was also reported by Alfelali et al.¹⁶ in a study that included 197 subjects and where only 30% of diabetic patients benefited from at least one education session before the pilgrimage. It was suggested that a health education strategy is effective in improving knowledge and practice, as well as in reducing the incidence of health problems among pilgrims.¹⁷

Our study revealed also that the most common foot lesions among diabetic patients after returning from pilgrimage were hyperkeratosis (96.8%) and superficial fungal infections (61.3%). A foot ulcer was noted in three cases. In the study of Alfelali et al.,¹⁶ blisters and erythema were the most common lesions in diabetic as well as non-diabetic patients. In addition, hyperkeratosis was comparatively more frequent in diabetic pilgrims and more likely to be complicated by a foot ulcer. The absence of blisters and erythema lesions in our study group may be attributed to the timing of the clinical examination, which occurred 15 days to one month after the return of pilgrims from Hajj.

Regarding infections, fungal and bacterial ones are reported to be more prevalent, particularly in pilgrims with unbalanced diabetes and unhealthy lifestyles.¹⁸ Fungal foot infections were found to be more common in patients taking anti-diabetic medications compared to those using insulin.¹⁹ However, in our research, fungal infections were found to be only linked to a history of inter-toe infection or onychomycosis. There was no correlation between these infections and diabetes control, or treatment used.

The conducted survey did not reveal any significant correlations between the occurrence of foot ulcers and the duration of diabetes, gender, insulin intake, body mass index, average A1C levels, or a history of foot ulcers. This aligns with findings from several studies showing the absence of a correlation between the duration of diabetes, insulin treatment, weight excess, and foot ulcer development.^20,21 Other studies reported that men and history of foot ulcers did raise the risk of developing foot lesions and that risk was tripled in case of A1C level beyond 9%.^22–24

However, our study has shown an association between the occurrence of a foot ulcer and lipid profile abnormalities. In fact, patients, who had a foot ulcer, had significantly lower total cholesterol and LDL cholesterol levels, this could be explained by the fact that these patients were at high cardiovascular risk and were already on statin therapy. They also had a higher triglyceride level and a lower HDL cholesterol rate. Even so, in multivariate analysis, no factor was significantly correlated with a higher risk of foot ulcer. The correlation between the occurrence of a foot ulcer and total cholesterol level was reported in the study by Porciúncula et al.²⁵ Nevertheless, a correlation with other abnormalities in the lipid profile has not been demonstrated.^25,26

The small sample size and the loss to follow-up after returning from pilgrimage were the main limitations of our study. The assessment of microvascular diabetes complications among pilgrims was not conducted due to time constraints.

In summary, the Hajj pilgrimage poses a potential risk of foot injuries for diabetic pilgrims, which could significantly impact their health and well-being. Therefore, an assessment of all patients before the pilgrimage is necessary, not only to ensure glycemic control but also to prevent diabetes-related complications. Prioritizing education on podiatric care is essential for diabetic patients who are considering the pilgrimage to mitigate the risk of foot-related complications and guarantee a successful pilgrimage experience.