Original Paper Received: September 16, 2015 Accepted: January 14, 2016 Published online: February 5, 2016

Neuroepidemiology 2016;46:173–181 DOI: 10.1159/000444056

Prevalence of Diabetes and Diabetic Neuropathy in Qena Governorate: Population-Based Survey Eman M. Khedr a Gharib Fawi c Mohammed Abd Allah Abbas d Noha Abo El-Fetoh a Ghada Al Attar b Ahmed F. Zaki d Ayman Gamea d   








Department of Neuropsychiatry and b Department of Public Health and Community Medicine, Faculty of Medicine, Assiut University, Assiut, c Department of Neuropsychiatry, Faculty of Medicine, Sohag University, Sohag, and d Department of Neuropsychiatry, Faculty of Medicine, South Valley University, Qena, Egypt  




Abstract Background: No previous study was done to estimate the prevalence of diabetic neuropathy (DN) in Arabic countries. The aim of this study was to estimate the prevalence of DN and its characteristics in Qena governorate. Material and Methods: This is a random sampling of 10 study areas, involving 9,303 inhabitants; 51.1% men and 48.9% women were recruited. There were 57.3% urban residents and 42.7% rural residents. Patients were diagnosed using a screening questionnaire for diabetes mellitus (DM) as well as for DN in addition to measuring blood sugar in suspected cases. All positive cases were referred to Qena University Hospital and were subjected to full clinical, electrophysiological and laboratory investigations. Results: Out of 9,303 people screened, 837 were diabetic giving prevalence 8.99% of the population. Eight hundred eleven had type II DM and 26 cases had type I giving prevalence of 8.7 and 0.3%, respectively. One hundred fifty-five out of 837 (18.5%) diabetic patients had evidence of DN with prevalence rate being 1.7% of the total

© 2016 S. Karger AG, Basel 0251–5350/16/0463–0173$39.50/0 E-Mail [email protected] www.karger.com/ned

population. Diabetic polyneuropathy was the commonest type with prevalence 1.5%. The prevalence of DN was higher in women than in men. Rural residents had significantly higher prevalence of DN compared to urban residents (1.9 vs. 1.4) and illiterate population more than educated (5.8 vs. 1.2). Conclusion: The overall crude prevalence rate of DM and DN is nearly the same as in European countries and lower than that in other Arabic countries. © 2016 S. Karger AG, Basel


Diabetes is a major clinical and public health problem worldwide. In 2013, 382 million people had diabetes, and it is estimated that 592 million people will be affected by 2035 [1]. The impact of this global burden is highest in low and middle income countries. In Egypt, 15.6% of the population was estimated to have diabetes in 2013, which is the second highest prevalence rate in the Middle East and North Africa region after Saudi Arabia. This percentage is expected to increase to 18.6% in 2035 [1]. In a crosssectional study that was conducted in Cairo, it was estimated that the combined prevalence of diagnosed and Prof. Dr. Eman M. Khedr Faculty of Medicine, Department of Neuropsychiatry Assiut University Hospital and Director of Neuropsychiatric department Aswan University Hospital, Assiut (Egypt) E-Mail emankhedr99 @ yahoo.com

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Key Words Egypt · Epidemiology · Prevalence · Peripheral neuropathy · Diabetes mellitus · Diabetic neuropathy

Subjects and Methods Study Population This is part of a cross-sectional community-based study that was implemented to estimate the prevalence of neuromuscular disorders in Qena governorate. Here, the Nile valley is at its narrowest in Egypt and the arable land, a green strip only 1 or 2 km on either side of the river is bordered by barren desert on both sides. Qena is an agricultural and industrial governorate.


Neuroepidemiology 2016;46:173–181 DOI: 10.1159/000444056

The sample size was based on an expected prevalence of 0.4%, with a 2 percentage point error and a 95% CI, allowing for a 10% refusal to participate. The study was conducted over a period of 2 years from September 1, 2013, to August 31, 2015. Any positive subject fulfilling the diagnostic criteria of DN at any time of their lives was considered as a prevalent case (new and old cases), and any subject who gave a history suggestive of DN developing during the period of the survey was considered an incident case (new cases diagnosed during the study period) of DN. Sampling Methodology A multistage random sample was applied where the governorate consists of 2 cities and 11 districts. Districts were divided into 3 groups according to their geographic location from the Nile (East, West and North) where 1 district was randomly chosen within each geographic area. Six rural areas (2 villages within each district) and 4 urban areas (2 areas within each city) were selected via simple random sampling, then each study site was subdivided into 4 areas and the most safe and secure area was chosen. Later, households were selected via systematic random sampling. First Stage: Selection of Study Areas and Sampling of Households According to the preliminary results of the 2006 census, Qena population is about 3 million; 21.4% of them live in urban areas and 78.6% in rural areas. Qena governorate consists of 2 cities (Qena and Nagh Hammadi, both considered as urban areas) and 11 districts (considered as rural areas and distributed around the Nile, where most of the people were farmers). According to the geographic location from the Nile, that is, East Bank, West Bank and North Bank, 1 district was randomly selected within each group with a total of 3 districts. Then, 2 villages (using simple random technique) were selected from each district. The 3 district areas were Nagada (in the West Bank of the Nile), Qift (in the East Bank of the Nile) and Dishenna (in the North Bank of the Nile) with a total of 6 villages considered as rural populations. We selected 2 urban areas from each city (Qena and Nagh Hammadi), with a total of 4 urban areas using simple random technique. Each selected village or area was then subdivided into 4 areas, and we chose the safest and easiest one to reach. Selection of the Households. A systematic random sample of households in the 10 areas was then applied by selecting every third household in each of the 10 study areas. A total of 9,303 individuals (1,057 families) from all ages were successfully interviewed out of 9,980 inhabitants (1,276 families). The response rate was 93% where 677 inhabitants could not be examined as they were not staying at the governorate at the time of survey. It is also noteworthy to mention that 69 families refused to participate; however, each was replaced by the next-door family. The total population included 5,334 and 3,969 living in urban and rural areas, respectively. Ethical approval for the study was obtained from the Ethical Committee of the faculty. Second Stage: Screening and Detecting of Positive Cases Initial diagnosis was based upon a general 2-part screening questionnaire with Part I recording sociodemographic information and Part II involving: (a) A screening questionnaire for diagnosis of DM according to the diagnostic criteria of the 2006 WHO recommendations,

Khedr/Fawi/Allah Abbas/El-Fetoh/ Al Attar/Zaki/Gamea

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undiagnosed diabetes in the Egyptian population ≥20 years of age was 9.3% [2]. Moreover, in another study, it was estimated that diabetes affected 7.5% among Egyptians aged 20–79 years in 2013 [1]. Diabetic peripheral neuropathy (DPN) is a common complication of diabetes mellitus (DM) and may affect one-third to over two-thirds of patients, depending upon the population characteristics, diabetes duration and diagnostic methods [3]. Although all types of peripheral nerves can be involved, it is usually sensory dominant with eventual involvement of motor nerve fibers [4]. Diabetic neuropathy (DN), which may be focal or diffuse, is diagnosed when diabetic patients complain of symptoms and/or show signs of peripheral nerve dysfunction after the exclusion of other etiologies [5, 6]. As for Arab countries, Saudi Arabia recorded the highest prevalence of DN (82%) with 57% asymptomatic patients [7] followed by Libya (45%) [8] and United Arab Emirates (34.7%) [9]. Chronic sensorimotor DPN is the most common form of DN [10, 11]. Herman et al. [2] reported that 22% of diabetic patients have a neuropathy. Among diabetic patients attending out-patient clinics in Alexandria, 38 and 29% of patients had not received a fundal or neurologic examination, respectively [12]. Due to its insidious onset, it has been estimated that the onset of non–insulin-dependent DM (NIDDM) occurs 7.6 years before clinical diagnosis [13]. Thus, it is important for the MOHP to conduct screening tests especially among vulnerable groups. Periodic fundal, neurologic and foot examination are necessary to safeguard against diabetic complications [12]. Moreover, in Egypt, the quality of diabetes care differs in many aspects from the recommended standards [12]. Most previous diabetic studies in Egypt focused on prevalence of diabetes in general [2, 12–14], while others focused on interventions [15]. However, very little is known about the prevalence of diabetes and its complications in many countries. This study aims to estimate the prevalence of diabetes and DN in Qena governorate/Egypt.

Third Stage: Confirming Positive Cases on Screening and Evaluation of Positive Cases Subjects who screened positive were referred to the hospital to be clinically evaluated and investigated. Diagnosis was confirmed using laboratory examinations (serum fasting and 2 h blood sugar assessment, glycosylated hemoglobin as well as renal and hepatic functions, thyroid function (T3, T4, and TSH), erythrocyte sedimentation rate and urine analysis to exclude other cause of neuropathy). Any participant known to have diabetes was classified based on the patient’s age at diagnosis, history of ketoacidosis and management into either type I if the patient had been diagnosed before 30 years of age and had been using insulin with or without a history of diabetic ketoacidosis or type II if the patient had been diagnosed after 30 years of age with an elevated blood glucose that was currently being managed with diet alone or with oral hypoglycemic agents with or without insulin and with no history of diabetic ketoacidosis.

DN in Qena/Egypt

Nerve conduction (sensory and motor) including F-wave latencies and H reflexes as well as electromyography of muscles of upper and lower limbs was performed for each case to confirm the diagnosis of peripheral neuropathy. The normal limits of motor conduction velocities, distal latencies, conduction times and latencies of F-wave and H reflex were set at +2 SD from the mean values of the healthy subjects. The CMAP was considered abnormal if the peak-to-peak amplitude was below the lowest value found in the healthy subjects. F-waves from both upper and lower limbs were recorded to median, ulnar, common peroneal and posterior tibial nerves using supramaximal stimulation with surface electrode at the belly of appropriate muscles. The ground electrode was placed on the forearm or leg between the stimulating and recording electrodes. Twenty trials for F-wave and H reflex of each nerve were recorded and the mean F-wave latency was measured. Skin temperature was controlled. Recordings were performed with a Nihon Kohden equipment (model 7102) with the following parameters: sweep time 8 ms/D, sensitivity 0.5 mV/D, low frequency filter 2 Hz, high frequency filter 10 kHz, stimulation duration 0.1 ms and stimulation frequency 1 Hz. Magnetic resonance imaging of cervical and lumbosacral regions was performed if needed to exclude cervical or lumbosacral spondylosis. Ninety age and sex matched healthy volunteers were recruited from the field of the study to be used as a control group for neurophysiology. Statistical Analysis An electronic data entry file was prepared. Data were entered using a simple spread sheet (Excel Program). Analysis followed after data verification and correction using SPSS version 16. The distribution and different subtypes of neuropathy are presented as prevalence rate in the population, together with specific rates, for example, age-specific rates, residence- and gender-specific prevalence rates.


Out of the 9,303 individuals screened, 837 cases were diabetic with a CPR of 9/100 population (546 subjects known to be diabetic and 291 subjects newly diagnosed during the survey). Eight hundred and eleven out of 837 cases had type II DM and 26 cases had type I with CPRs of 8.7/100 and 0.3/100, respectively. A total of 155 (18.5%) out of 837 diabetic patients had clinical and neurophysiological evidence of DN giving a CPR of 1.7/100 of the total population and 38.5% among type I diabetic patients (10 out of 26 patients) and 17.9% among type II diabetic patients (145 out of 811 patients), p < 0.05 (table 1). One hundred and forty cases (16.7% of diabetic patients) were suffering from chronic sensorimotor polyneuropathy according to the Michigan screening instrument (either through questionnaire and/or a lower extremity examination) and confirmed by neurophysiNeuroepidemiology 2016;46:173–181 DOI: 10.1159/000444056


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which tests for symptoms of diabetes (polyuria, polydipsia, unexplained weight loss) plus plasma glucose concentration ≥200 mg/ dl or fasting plasma glucose ≥7.0 mmol/l (126 mg/dl) or 2 h plasma glucose ≥11.1 mmol/l (200 mg/dl). (b) The Michigan Neuropathy Screening Instrument (MNSI) [16] was used for evaluation of peripheral neuropathy in diabetes. The MNSI includes 2 separate assessments, a 15-item self-administered questionnaire that is scored by summing abnormal responses and a lower extremity examination that includes inspection and assessment of vibratory sensation and ankle reflexes and is scored by assigning points for abnormal findings. All items on the questionnaire were coded as 0 for a negative response and 1 for a positive response. For the examination, responses for the left and right feet were combined. For each measure of the examination (appearance, ulcer, reflex and vibration), a combined score of ≥1.0 was classified as abnormal. Neuropathy is defined operationally as ≥7 positive responses on the MNSI questionnaire or a score >2.0 on the MNSI examination and thresholds defined by prior validation studies. Patients who did not reach these thresholds but were suspected to have neuropathy were also referred to the hospital for neurophysiological studies. The screening questionnaire of MNSI was pretested in an outpatient clinic on a sample of 30 DN patients and 30 age- and sexmatched family members who had joint pain without manifestations of DM or neuropathy to test the Arabic translated version of the questionnaire and to train the data collectors. The sensitivity and specificity of the questionnaire were 97 and 86%, respectively. A special questionnaire and examination to detect other types of diabetic neuropathies (cranial nerve palsy, truncal neuropathy and diabetic amyotrophy) was also given to each diabetic patient. The survey team comprised of 3 social workers (at least 10 years of school education) who applied the screening questionnaire headed by a neurologist (master degree with at least 3 years of experience), who confirmed the diagnosis by applying the screening questionnaire and referring the positive cases to the Qena University Hospital. The social workers received 3 weeks of training on how to collect the data using the screening tool before starting the study. A written consent was obtained from study participants prior to enrolling in the study.

Table 1. CPR of DM and DN in Qena governorate



95% CI

DM Diabetic patients type I Diabetic patients type II Total DN DN in type I DN in type II

837/9,303 26/9,303 811/9,303 155/9,303 10/9,303 145/9,303

8.99 0.28 8.72 1.67 0.11 1.56

8.39–9.61 0.172–0.387 8.12–9.32 1.40–1.93 0.041–0.174 1.305–1.812

Types of DN Distal symmetric sensorimotor polyneuropathy Cranial neuropathy 3rd nerve palsy 6th nerve palsy Facial palsy Mononeuritis multiplex Diabetic truncal neuropathy Diabetic amyotrophy

140/9,303 8/9,303 3/9,303 3/9,303 2/9,303 3/9,303 2/9,303 2/9,303

1.51 0.86 0.03 0.03 0.02 0.03 0.02 0.02

1.256–1.754 0.026–0.146 0–0.069 0–0.069 0–0.051 0–0.069 0–0.051 0–0.051

DN according to sex Female Male

71/4,751 84/4,552

1.49 1.84

1.147–1.842 1.451–2.240

DN according to residence Urban Rural

76/5,334 79/3,969

1.43 1.91*

1.10–1.75 1.55–2.43

DN according to education Illiterate/read and write# Educated

85/1,478 70/5,752

5.75*** 1.22

4.53–6.97 0.93–1.50

Crude incidence rate of DN Male Female

14/9,303 7/4,751 7/4,552

0.150 0.147 0.154

0.07–0.23 0.04–0.26 0.04–0.27

8/5,334 6/3,969

0.150 0.151

0.05–0.25 0.03–0.27

DN incidence according to residence Urban Rural # Two

thousand seventy-three childrens below the level of education. * The CPR of DN in rural vs. urban with p < 0.05. *** The CPR of DN among illiterate/read and write vs. educated, p < 0.0001. DM = Diabetes mellitus; DN = distal neuropathy.


Neuroepidemiology 2016;46:173–181 DOI: 10.1159/000444056

ropathy in neurophysiological study. The suspicious criteria include wasting and weakness of quadriceps muscle, the presence of girdle pain (truncal neuropathy or the hesitancy of patient response to the questionnaire. Three out of 10 cases diagnosed as mononeuritis multiplex (0.36% of diabetic patients), 2 had femoral amyotrophy and 2 had truncal neuropathy (0.24% of diabetic patients). The other 3 cases did not have any type of neuropathy. Eight cases were diagnosed with cranial neuropathy (1% of diabetic patients): 3 cases had 3rd nerve palsy and 3 had 6th nerve palsy (0.36% of diabetic patients), while Khedr/Fawi/Allah Abbas/El-Fetoh/ Al Attar/Zaki/Gamea

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ological study giving a CPR of 1.5%. Three cases had false positive findings using the Michigan questionnaire but these were eliminated because of negative findings on neurophysiology and lower limb examination. False positives are people who scored >7 but do not have neuropathy. These were identified by detailed clinical neurophysiology. Another 10 suspected cases had positive findings on neurophysiology although they had scored negatively on the Michigan score (‘false negative’). False negatives are people who scored

Prevalence of Diabetes and Diabetic Neuropathy in Qena Governorate: Population-Based Survey.

No previous study was done to estimate the prevalence of diabetic neuropathy (DN) in Arabic countries. The aim of this study was to estimate the preva...
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