Prevalence of Parkinsonism and Parkinson’s disease in Qena governorate/Egypt: a cross-sectional community-based survey Eman M. Khedr1, Gharib Fawi2, Mohammed Abd Allah Abbas3, Talal A. Mohammed3, Noha Abo El-Fetoh1, Ghada Al Attar4, Ahmed F. Zaki3 1

Faculty of Medicine, Department of Neuropsychiatry, Assiut University, Egypt, 2Faculty of Medicine, Department of Neuropsychiatry, Sohag University, Egypt, 3Faculty of Medicine, Department of Neuropsychiatry, South Valley University, Qena, Egypt, 4Faculty of Medicine, Department of Public Health and Community Medicine, Assiut University, Egypt Background and purpose: In a previous study we found a high crude prevalence rate (CPR) for Parkinson’s disease (PD) in Assiut governorate/Egypt. We therefore surveyed a second Nile valley governorate (Qena) to provide confirmatory evidence for the high prevalence rate of PD in Egypt. Subjects and methods: 10 areas in Qena governorate were selected by random sampling to recruit 8027 inhabitants. Positive cases were identified using a modified screening questionnaire, the unified Parkinson disease rating scale (UPDRS), mini-mental state examination (MMSE) and the non-motor symptoms scale (NMSS) for PD. Results: Forty-four patients were identified with Parkinsonism, giving a CPR of 548/105 inhabitants. Among them, 35 patients were diagnosed as PD with CPR of 436/105; three cases were diagnosed as drug-induced Parkinsonism with CPR 37/105; two cases had atherosclerotic Parkinsonism with CPR 25/105.Age-specific CPR of PD among population aged i50 years old was 2534/105.The highest age-specific CPR was recorded among subjects i75 years old. The CPR showed a tendency to be higher in males than females, urban than rural areas and industrial than non-industrial areas (503 vs 363/105, 474 vs 389/105 and 655 vs 312/105, respectively). There was a significantly higher CPR among illiterate than literate persons (1982 vs 299/105 with P50.00001). About one quarter of patients had cognitive impairment. All cases had positive symptoms in at least one or more NMS Domains. Conclusion: The overall prevalence of PD disease is high in Nile valley governorates of Upper Egypt compared to other Arabic countries.

Keywords: Parkinson’s disease, Prevalence, Dementia, Non-motor symptoms

Introduction Parkinson’s disease (PD) is the second most common neurodegenerative disorder after Alzheimer’s disease.1 It is characterised by motor (bradykinesia, rigidity and resting tremors) and non-motor symptoms (cognitive impairment, autonomic, affective and behavioural disturbances)2 and affects 1–2% of the population over the age of 60 years, with a much lower incidence in younger individuals.3 The population in less developed regions is ageing more rapidly than in the developed world and is expected to increase by a factor of 3 in the next four decades.4 Consequently, the burden of PD will increase dramatically and the most significant changes are

Correspondence to: Eman M. Khedr, Department of Neurology, Assiut University Hospital, Egypt. Email: [email protected]

ß W. S. Maney and Son Ltd 2015 DOI 10.1179/1743132815Y.0000000020

expected to occur in healthcare systems of less developed countries. Many epidemiological studies have been conducted worldwide over the past few decades. The prevalence of PD varies among different ethnic and geographic regions around the world. In door-to-door studies, the rate of crude PD prevalence was found to be as low as 15/105 for all ages in China5 and as high as 1990 and 3333/105 for population at risk (w64 years) in Spain6 and Brazil (Bambuı´ study).7 However, few epidemiological studies have been conducted in Arabic countries. Recently, three studies8–10 have been published from Egypt. The results varied over a wide range, giving a crude prevalence rate (CPR) of PD from 213.15 to 2748/105 among the population aged i40 or i50 years. Nevertheless these rates are high compared to those in other Arabic countries.

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Prevalence of Parkinson’s disease in Qena/Egypt

We, therefore, performed a second door-to-door survey in the mixed industrial/rural Nile governorate of Qena in Upper Egypt to provide additional confirmatory evidence for the high prevalence rate of PD. We hope that estimation of PD frequency in Egyptian populations of different governorates (Assuit and Qena governorates represent 4.7 and 4.1% of Egypt’s population, respectively (3 441 597 and 3 001 494/72 579 030 according to Census 2006 data11), will provide data for a management plan of PD to ameliorate quality of life and socioeconomic burden among old people and caregivers in Egypt.

Methods Study population A cross-sectional community-based study was implemented 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. It is an agricultural and industrial governorate. There are three industrial zones in the governorate (one is situated at Qift and two zones in Nagh Hammadi) where there are sugarcane factories, aluminium (Al) processing, spinning and weaving, food and paper factories as well as fabricated metals and non-metallic mineral production. The Al complex is one of the largest industrial concerns in the Middle East. The sample size was based on an expected prevalence of 0.4%, with a 2% point error and a 95% confidence interval (CI), allowing for a 10% refusal to participate. The study was conducted over a 2-year period from 1 September 2011 to 31 August 2013. The prevalence day in the present study was 31st August 2013.

Sampling methodology Stage I: selection of study areas and sampling of households Details of selection of the study sites are given in our previous study.12 First, according to the geographic location we selected three districts randomly out of a total of 11 districts, and then we selected two villages (areas) from each district. The three district areas were: Nagada (in the west bank of Nile), Qift (in the east of Nile) and Dishenna (in the north bank of the Nile) with a total of six villages considered as rural populations. We selected two urban areas from each city (Qena city and Nagh Hammadi city), with a total of four urban areas using simple random technique and according to local security safety. Selection of the households: a systematic random sample of households in the 10 areas was then taken by selecting every third household in each of the 10 study sites.

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Stage II: screening and detecting of positive cases Initial diagnosis was based on a general two-part screening questionnaire with Part I recording sociodemographic details and Part II involving a PD screening questionnaire13 translated into Arabic and applied previously in the Assiut governorate survey.8 The screening questionnaire consisted of eight questions, and each question had a yes or no answer. Question 1 inquired about tremors, questions 2, 5, 7 and 8 inquired about bradykinesia, question 6 inquired about balance and questions 3 and 4 inquired about rigidity and changes in speech or writing quality (in educated participants) in the recent past. The sensitivity and specificity of the questionnaire were 95% and 85%, respectively. The survey team comprised 10 social workers (at least 10 years education level) who applied the screening questionnaire headed by a neurologist and psychiatrist (masters degree with at least 5 years of experience), who confirmed the diagnosis by re-applying the screening questionnaire and referring the positive cases to Qena University Hospital. The team workers received 3 weeks of training on how to carry out the protocol before starting the study. Third stage: confirming positive cases on screening and evaluation of positive cases Fifty-one subjects who screened positive were selected and referred to hospital to be fully evaluated and investigated. Forty-four out of 51 fulfilled the UK Parkinson’s Disease Society (UKPDS) Brain Bank Criteria14 for a diagnosis of Parkinsonism/PD. These criteria require the presence of bradykinesia and at least one other feature of Parkinsonism (rigidity, tremors or impaired balance). Seven cases were excluded: three patients were diagnosed with osteoarthritis, two cases had spastic quadriparesis secondary to cervical spondylosis and one case had spastic quadriparesis 2 years following a double stroke and another case had senile tremors. A full clinical medical history was taken by a neurologist from Qena university hospital, Neuropsychiatric department of all cases. Neuroimaging (computerised tomography and magnetic resonance imaging) was performed for all patients and electroencephalography for suspected cases of post-encephalitic Parkinsonism. Laboratory measures of copper and ceruplasmin levels in serum and urine, liver functions and ophthalmalogical examination were included for suspected cases for Wilson’s disease. Metabolic tests included blood sugar, urea and creatinine. The diagnosis of idiopathic PD is based on the presence of two or more of the four cardinal signs and a response to L -dopa therapy.15 History and other investigations identified patients with secondary Parkinsonism, e.g. drug-induced Parkinsonism, vascular Parkinsonism, corticobasal ganglionic degeneration or Wilson’s disease. Vascular Parkinsonism was

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identified by atherosclerotic manifestations (history of stroke, computerised tomography of the brain showed infarction, focal neurological deficit and others).16 Drug-induced Parkinsonism was identified in patients in whom there was no history of Parkinsonism before the use offending drug (antipsychotic, antiemetic or others), and onset of Parkinsonian symptoms during the use of offending drug.17 Post-encephalitic Parkinsonism was classified as Parkinsonism following encephalitis (sleeping sickness, oculogyria and its characteristic sequelae).18 Possible corticobasal ganglionic degeneration syndrome (CBS) was made on the basis of DSM IV criteria for diagnosis of CBS in which core features are a progressive asymmetrical akinetic-rigid syndrome and associated higher cortical signs, most prominently ideomotor apraxia19–21 with a postural or action tremors and sometime unilateral dystonia. The Parkinsonism of CBS characteristically fails to respond to levodopa.20–22 Wilson’s disease was diagnosed on the basis of a combination of Parkinsonism features with liver cirrhosis, Kayser-Fleischer rings23 in the cornea and reduced serum ceruloplasmin and copper level24 plus or minus elevated copper level in 24 hours urine exceed 100 mg/day.25,26 Each case was evaluated using the mini-mental state examination (MMSE),27 unified Parkinson disease rating scale (UPDRS-III),28 Hoehn and Yahr29 staging and non-motor symptoms scale (NMSS).30 People fulfilling the diagnostic criteria of Parkinsonism/PD prior to the prevalence day (31 August 2013) at any time of their lives were considered as prevalent cases, and any subject who gave a history suggestive of PD developing during the period of the survey was considered an incident case of PD.

Statistical analysis Different scales were reviewed, and open-ended questions were coded and entered using a simple spread sheet. Analysis followed after data verification and correction. All data were analysed with the aid of the Statistical Package for the Social Sciences (SPSS) ver. 16 (www.spss.com). The results are expressed as mean + SD.

Results Out of a total of 8760 inhabitants (1076 families), 733 inhabitants could not be examined (away from governorate at the time of survey), giving a final sample of 8027 inhabitants (1076 families). Forty families refused to participate; each one was replaced by the next door family in the survey. In the present survey, 44 patients were diagnosed with Parkinsonism, giving CPR of 548/105 inhabitants of studied population. Of these, 35 cases were diagnosed as PD, giving a CPR of 436/105 inhabitants. The remaining nine cases were diagnosed as

Prevalence of Parkinson’s disease in Qena/Egypt

follows: three cases had drug-induced Parkinsonism (with CPR 37/105 inhabitants), two had vascular Parkinsonism, two had possible corticobasal ganglionic degeneration (CPR 25/105 inhabitants in both cases), one had post-encephalitic Parkinsonism and one had Wilson’s disease (CPR 12/105 inhabitants in both cases) (see Table 1). The CPR of PD was slightly higher among males than females (503 vs 363/105; with P50.43 and OR51.39; 95% CI50.70–2.73) and in urban compared with rural areas (474 vs 389/100 000 with P50.68, OR51.22 95% CI50.62–2.40). It was significantly higher in industrial than in non-industrial areas (655 vs 312/105 with P50.039; and OR52.11; 95% CI51.08–4.10) and among illiterate than literate individuals (P50.0001; OR56.73; 95% CI53.43– 13.2). Only five cases were newly diagnosed with PD during survey giving crude incidence rate 62/105 with male to female ratio 4:1 (see Table 1). The PD rates among those aged i50 years according to sex and residence are given in Table 2. No cases were recorded below 50 years old. The age- and sex-specific CPR of PD every 5 years for the 1381 inhabitants who were aged i50 years are shown in Table 3. The highest age-specific prevalence rates were in elderly subjects aged i75 years (15 094/105) (P50.00001). In the 35 patients with confirmed PD, the mean duration of illness was 2.75+ 1.3 years. Five patients (14.2%) had positive family history. All of the patients had bradykinesia; rigidity and resting tremors were recorded in 97 and 91.4%, respectively. Twenty-five patients received regular anti-Parkinsonian drugs, five patients received non-specific drugs (analgesic, anabolic and muscle relaxants) and five patients did not receive any anti-Parkinsonian drugs as they were newly diagnosed during the survey. Five cases had mild dementia (14.3%). The PD patients living in industrial areas were younger and had earlier age of onset and shorter duration of PD than those in non-industrial areas (P50.026, 0.044, 0.001), respectively (Table 4). All PD patients reported at least positive one domain in the NMS scale. The highest frequency was found with Gastrointestinal tract domain (GIT) domain and the least in perceptual problems (100 and 11.4%, respectively). No significant difference was found between frequency of NMSS domains in relation to sex or residence (Table 5).

Discussion In the present study, the CPR of PD was 436/105 for all ages which is similar to that reported in a previous study (557/105 and 2748/105 for all ages and subjects aged i50 years old, respectively) in Assiut, Egypt.8 Both of

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Table 1 Crude prevalence rate of PD and other Parkinsonism among total studied population CPR (number of cases/number of population ‘all ages’) CPR of Parkinsonism (44/8027) CPR of PD (35/8027) Drug-induced Parkinsonism(3/8027) Vascular (atherosclerosis) Parkinsonism (2/8027) Wilson disease (1/8027) Post-encephalitic Parkinsonism (1/8027) Corticobasal ganglionic degeneration (2/8027) CPR of PD among sex distribution Male (21/4172) Female (14/3855) CPR of PD in relation to residence Urban 21/4427 Rural 14/3600 CPR of PD in relation to industrial vs non-industrial Industrial 19/2900 Non-industrial 16/5127 CPR of PD in relation to education Illiterate 15/757 Literate 20/6680 Crude incidence rate of PD (5/8027) Crude incidence rate of PD for males (4/4172) Crude incidence rate of PD for females (1/3855)

CPR/100 000

95% CI

548 436 37 25 12 12 25

386–710 292–580 0–80 0–59 0–37 0–37 0–59

503 363

288–719 173–553

474 389

271–677 185–593

655* 312

361–950 159–465

1982** 299 62 96 26

979–2984 168–431 8–117 2–190 0–77

Five hundred and ninety subjects out of education age; CPR: crude prevalence rate; PD: Parkinson’s disease; CI: confidence interval. *Pv0.05 ** Pv0.0001.

these governorates lie along the Nile and have higher prevalence rates than in two other Egyptian governorates outside the Nile valley (Al-Kharga Valley [desert governorate] and Al Qusier [governorate along the Red Sea]9,10 which recorded CPRs of 213.15 and 452.1/105, respectively, among those aged i40 years. Table 2 Crude prevalence and incidence rates of PD among population at risk (i50 years) in relations to sex, residence, industrial areas and educational state Age-specific rate (number of cases/number of population at risk i50 years) Age-specific prevalence rate among sex Male (21/675) Female (14/706) Age-specific rate in relation to residence Urban 21/710

95% CPR/100 000 CI 2534

1695–3374

3111 1983

1780–4442 944–3022

2958

1693– 4223 993–3179

Rural 14/671 2086 Age-specific rate in relation to industrial vs non-industrial areas Industrial 19/400 4750*** Non-industrial 16/981 1631 Age-specific rate in relation to education Illiterate 15/483 3106 Literate 20/898 2227 Age-specific incidence rate of 362 PD (5/1381) Age-specific incidence rate of 593 PD in males (4/675) Age-specific incidence rate of 142 PD in females (1/706) CPR: crude prevalence rate; PD: CI: confidence interval. *** Pv0.001.

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1534–4677 1251–3203 45–679 12–1173 0–419 Parkinson’s

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disease;

Overall, the prevalence of PD in Egypt is higher than in other Arabic countries that employed door-to-door surveys (27–43/105) such as Saudi Arabia,31 Libya32 and Tunisia33 as well as in Arab Israel (43.24/105).34 Different diagnostic criteria, different environmental influences, lack of investigatory tools, the different age-specific group and the sample size may contribute to some of these differences in PD prevalence. The incidence rate of PD in Assiut and Qena were 82 and 62/105 (all ages), respectively, but this was not recorded in other Egyptian and Arabic studies. Overall, the high CPR and incidence rate of PD in Assiut and Qena governorates/Egypt may be related to the presence of industrial zones within the cities especially in Qena which has many factories concerned with Al refining as well as sugar refining, manganese production, paper making and building materials. The sewage from these factories drains to some extent into the Nile or its water canals and could increase the risk of exposure to toxins compared to other areas studied far away from the Nile Valley. In Salem et al.35 study, they collected water samples randomly from Aswan, Qena, Assiut and Beni Suef cities. They found that manganese values were above WHO MCL (0.5 mg/l) in 30% of samples from Qena city only. This data could explain partially the high CPR of PD in Qena. Manganism is a disease characterised by excessive brain manganese deposition and shares multiple features with PD. In the early stages of the disease, patients with manganism display psychotic symptoms, which progress to chronic symptoms associated with disturbances in extrapyramidal circuits, such as akinetic rigidity, dystonia and

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Table 3 Crude prevalence rate of Parkinson’s disease with age and sex specific groups of PD in Qena governorate, Egypt

Demographic data

Number of cases

Age-specific CPRi50 years Total 35 Male 21 Female 14 F/M ratio51/1.4 50–54 years Total 2 Male 1 Female 1 55–59 years Total 2 Male 1 Female 1 60–64 years Total 6 Male 4 Female 2 65–69 years Total 8 Male 5 Female 3 70–74 years Total 9 Male 7 Female 2 w75 years Total 8 Male 3 Female 5

Number of inhabitants (population at risk)

Percentage of studied population (n58027)

1381 675 706

17.2 8.4 8.8

2534 3111 1983

1695–3374 1780–4442 944–3022

313 156 157

3.9 1.9 2

639 641 637

0–1525 0–1897 0–1885

377 179 198

4.69 2.22 2.47

531 559 505

0–1266 0–1654 0–1495

337 163 174

4.19 2.03 2.16

1780 2454 1149

356–3205 49–4859 0–2742

211 101 110

2.63 1.26 1.37

3791 4950 2727

1164–6419 611–9290 0–5813

90 50 40

1.12 0.62 0.5

10 000 14 000* 5000

3467–16 533 3629–24 371 0–11 930

53 26 27

0.66 0.32 0.34

15 094** 11 538 18 519***

4634–25 554 0–24 595 2286–34 751

CPR/100 000

95% CI

CPR: crude prevalence rate; PD: Parkinson’s disease; CI: confidence interval; * Pv0.0001; the highest age-specific prevalence rate for males, ** Pv0.0001; the highest age-specific prevalence rate for both sex, *** Pv0.0001; the highest age-specific prevalence rate for females.

bradyskinesia.36,37 Neuronal loss and gliosis in the globus pallidus, the substantia nigra pars reticulata and the striatum characterise manganism at the morphological level.36 To compare between previous studies we selected those that recorded CPR according to age-specific groups (Table 6). The present study as well as our previous study8 (2534/105 and 2748/105, respectively for subjects aged i50 years) recorded the second highest CPR after Brazil (3333/105 CPR for population i65 years),7 followed by Spain,6 Italy38 and the Netherlands39 (1999, 1500 and 1400/105, respectively). This difference in recording CPR of PD in different studies could be related to different methodological approach, genetic susceptibility and inclusion criteria of studied community and selected sample. In the present study, age-specific prevalence rates of PD increased with age for both genders, with no cases recorded below age of 50 years. A preponderance of males was seen in most of the age groups but was not significant. This is consistent with all Arabic studies.31–33 Our recorded crude age and sex specific prevalence increased steadily with age up to w75 years as in other conducted studies.8,34,38–44 The lower incidence in women may be attributed partially to neuroprotective effect of estrogen,44,45 perhaps via inhibition of

dopamine transporter affinity and prevention of entry of neurotoxic agents into dopaminergic nerve terminals.45 Men may be more vulnerable because they are more likely to be exposed to environmental and occupational hazards of neurotoxic agents than women. The prevalence of PD in our urban population was slightly but not significantly higher than in the rural population (474 vs 389/105). However, in our previous study,8 we found the opposite. Industrial zones lie within urban areas in Qena while they are separated in Assiut, and this may explain the differences between the two studies. Our findings are consistent with reported data from Thailand,46 London47 and Estonia.48 However, Benito-Leo´n et al.49 reported no difference in CPR of PD between rural and urban areas among elderly population in central Spain. There was an earlier age of onset of PD among people living in industrial areas versus non-industrial areas. This finding may again be related to high-risk environmental factors for individuals who live in industrial areas where exposure to environmental heavy metal toxins is suspected. There is evidence suggesting that Al exposure may promote the onset of PD. Previously an epidemiological study has found a correlation between this disorder and Al exposure.50 Aluminium concentrations are elevated in dopamine-related brain

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Table 4 Demographic and clinical profile of 35 PD patients according to industrial vs non-industrial areas

Variables Age (years) Age of onset (years) Duration (years) Total UPDRS Hoehn and Yahr (HY) stage Total NMSS MMSE score Sex Male number (%) Female number (%) Positive family history Treatment Received specific treatment Received non-specific treatment New diagnosed and prescribed treatment Symptoms of PD Bradykinesia Resting tremors Rigidity Postural instability Mild cognitive impairment Mild dementia No cognitive impairment Hoehn and Yahr (HY) stage 1.55unilateral disease plus axial involvement 2.55mild bilateral disease with recovery on pull test 35mild to moderate bilateral disease, some postural instability and physically independent 45severe disability, still able to walk or stand unassisted

Industrial areas (N519) mean+ SD

Non-industrial (N516) mean+ SD

P-value

62.2+ 8.2(54–75) 59.6+ 7.8(52–77) 1.9+ 0.9(1–4) 23.5+ 6.7(9–35) 2.8+ 0.8(1.5–4) 16.9+ 12.5(5–42) 25.7+ 3.9(17–30)

68.3+ 7.2(50–75) 64.9+ 7.1(47–72) 3.3+ 1.3(1–5) 26.9+ 8.7(18–47) 2.7+ 0.8(2.5–4) 15.9+ 12.3(2–41) 23.4+ 3.7(17–30)

0.026 0.044 0.001 0.221 0.727 0.824 0.084

10(52.6%) 9(47.4%) 1(5.3%)

11(68.8%) 5(31.2%) 4(25%)

0.33

18(94.7%) 0(0%) 0(0%)

7(43.6%) 5(31.2%) 5(31.2%)

0.0006

19(100%) 17(89.5%) 18(94.7%) 19(100%) 1(5.3%) 2(10.5%) 16(84.2)

16(100%) 15(93.8%) 16(100%) 15(93.8%) 2(12.5%) 3(18.7%) 11(68.8%)

0.65

1(5.3%) 4(21%)

0(0) 7(43.7%)

0.38

11(57.9%)

6(37.5%)

3(15.8%)

3(18.8%)

0.042

0.27

UPDRS: unified Parkinson disease rating scale; NMSS: non-motor symptoms scale; MMSE: mini-mental state examination; PD: Parkinson’s disease.

Table 5 Frequency and percentage of occurrence of each domain of NMSS NMSS domains

Yes/(Percentage of positive cases)

Industrial/non-industrial N519/16 (%)

25/10(71.4) 26/9(74) 28/7(80) 4/31(11) 15/20(42.9) 35/0(100) 30/5(85.7) 20/15(57) 27/8(77) 35/0(100)

12/13(63.2/81.3) 14/12(73.7/75) 17/11(89.5/68.8) 4/0(21.1/0) 11/4(57.9/25) 19/16(100/100) 16/14(84.2/87.5) 11/9(57.9/56.3) 16/11(84.2/68.8) 19/16(100/100)

Cardiovascular Sleep/fatigue Mood/cognition Perceptual problems/hallucinations Attention/memory Gastrointestinal Urinary Sexual function Miscellaneous Total NMSS NMSS: non-motor symptoms scale.

regions of PD patients51 and occupational exposure to Al may constitute a risk factor for PD.52 Another possible contributing factor to the overall high CPR of PD in our community is the use of pesticides in rural areas that have been consistently implicated as one of the most likely major environmental risk factors for PD.53–55 This potential link has been particularly strong for organophosphates, organochlorines (especially used in indoor air urban and rural homes), rotenone and paraquat, partly due to a structural similarity between the neurotoxin 1-methyl-4-phenylpyridinium and these pesticides.56 Pesticide residues,

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especially organophosphate compounds, in soil, water and agricultural products, may be partly responsible for the increased numbers of patients with neurodegenerative disorders such as PD.54,57 Dawood et al.58 estimated organochlorine pesticide residues in samples of caw milk collected from Sohage and Qena governorates. The results of the study revealed that 82.5% were contaminated with one or more of the investigated organochlorine pesticides. The distribution was 95% of the samples from Qena and 70% from Sohag. Dichlorodiphenyltrichloroethane complex was the most frequent contaminant.

Drug tracer methodology

Masalha et al.34/Arabic Israel

Door-to-door, three-phase survey

Not stated

Ashok et al.32/Libya

Bergareche et al.65/Bidasoa, Spain

Door-to-door survey

Khedr et al.8/Assuit, Egypt

Screening questionnaire, neurological examination

Door-to-door survey

Tallawy et al.9/AlQuseir City, Egypt

Claverı´a et al.64/Cantalejo, Spain

Door-to-door survey

El-Tallawy et al.10/Al- Kharga district, Egypt

Door-to-door survey

Door-to-door survey

Khedr et al., the present study/Qena governorate, Egypt

de Rijk et al.39/Rotterdam, The Netherlands

Type of study

Author/country

Table 6 Crude prevalence rate with age-specific groups of PD among different studies

518 745/163

i2 cardinal signs: resting tremor, rigidity, hypokinesia, changes in postural/righting reflexes Individuals on anti-PD medication

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Parkinsonism: i2 out of four cardinal signs; PD calculated by using prevalence rates worldwide and pooled European cohort 1 sign documented in history improved by anti-Parkinsonian treatment and follow- up of cases PD: by exclusion of all other possible causes.

2,000 aged i 65 years/18

1,400 (i 55 years)

6,969 aged i 55 years/97

Europarkinson protocol criteria

2015

1,500 (i 65 years)

1,280 (i 60 years)

43.24 (all ages) 12.3 (v 65 years) 477.3 (i65 years)

31.4 (all ages)

111 (all ages) 451 (w40 years) 557 (all ages) 2748 (i50 years)

53 (all ages) 213.2 (i40 years)

436 (all ages) 2534 (i50 years)

115 000/49

The UK Parkinson’s Disease Society Brain Bank Criteria

33 283/37 8183 aged i40 years ears/37 5920/33

62 583/33 15 482 aged i40 years/33

8027/35

Diagnostic criteria given by the World Health Organization

According to Parkinson disease (PD) diagnostic criteria by Gelb et al.

The UK Parkinson’s Disease Society Brain Bank Criteria

Diagnostic criteria

Total Crude population/number prevalence/105 (age group) of cases

j35 years: NA 36–45 years: 13.65 46–55 years: 50.19 56–65 years: 132.2 66–75 years: 667.02 76–95 years: 290.2 55–64 years: 300 65–74 years: 1000 75–84 years: 3100 85–94 years: 4300 60–69 years: 630 70–79 years: 1300 80–89 years: 10 400 w90 years: 18 750 65–74 years: 400 75–84 years: 4700 w85 years: 2900

i50 years: 2748 j49 years: 0 50–59 years: 911 60–69 years: 2824 70–79 years: 7263 i80 years: 6250 i50 years: 285.1

i50 years: 2534 j49 years: 0 50–59 years: 580 60–69 years: 2555 i70 years: 11 888 i40 years: 213.15 40–49 years: 14 50–59 years: 47 60–69 years: 425 70–79 years: 1034 i80 years: 1896 i40 years: 452.1

Age-specific prevalence/105

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3 or more cardinal signs; alternatively, two cardinal signs were accepted as sufficient, provided all additional conditions were met.

Screened participants who took PD medications

Door-to-door survey

Door-to-door survey

Door-to-door survey

Door-to-door survey

Record-based General Hospitals, and Ministry of Welfare and Health

Zhang and Roman66/greater Beijing, China

Mehta et al.67/Australia

Chen et al.68/ Taiwan

Li et al.69/six cities, China

Wang et al.70/29 provinces, China

Tan et al.71/Singapore

Moriwaka et al.72/Hokkaido, Japan

Screening questionnaire, neurological examination

Screening questions, test for tandem gait, clinical examination

Morgante et al.40/Sicily, Italy

Kis et al.38/South Tyrol, Northern Italy

Type of study

Author/country

Table 6 Continued

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2 of four cardinal signs, negative brain CT scan, response to anti-Parkinsonian drugs and exclusion of secondary causes

National Institute of Neurologic Disorders and Stroke Criteria

Schoenberg’s criteria

Resting tremor and rigidity and/or hypokinesia and exclusion of other cause

at least two of the four cardinal signs of Parkinsonism

Follow-up a few months later to confirm the diagnosis of i cardinal signs; alternatively, two cardinal signs were accepted as sufficient, provided all additional conditions were met PD diagnosis was confirmed by contacting the participant’s medical/general practitioners

Europarkinson criteria

5 643 647/5342

15 000/46

3 869 162/566

63 195/28

11 332/80

3,509/16

5,743/64

750/12

i1 sign in treated patients; PD: by 19 955/63 exclusion of all other possible causes of Parkinsonism

Diagnostic criteria

Hokkaid 94.7 Iwamizawa: 95.8

290 (i50 years)

14.6 (all ages)

198 (i 50 years)

706 (i 40 years)

460 (all ages)

1,100 (i 55 years)

1500 (i 60 years)

257.2 (all ages)

Total Crude population/number prevalence/105 (age group) of cases 0–49 years: 0 50–59 years: 115.6 60–69 years: 621.4 70–79 years: 1978.3 80–89 years: 3055.0 60–64 years: 500 65–69 years: 1000 70–74 years: 600 75–79 years: 6500 80–85 years: 1100 55–64 years: 300 65–74 years: 1200 75–84 years: 3500 85–94 years: 3700 w95 years: 0 v60 years: 0 w60 years: 480 w70 years: 820 w80 years: 560 40–49 years: 0 50–59 years: 120.58 60–69 years: 686.91 70–79 years: 1837.89 w80 years: 4328.02 v50 years: 0 50–59 years: 92 60–69 years: 145 i70 years: 615 0–49 years: 0.7 50–59 years: 22.5 60–69 years: 89.4 70–79 years:157.6 i80 years: 132.4 50–59 years: 50 60–69 years: 280 70–79 years: 510 w80 years: 1250 40–49 years: 15.6 50–59 years: 79.8 60–69 years:241.8 70–79 years:800.7 i80 years: 358.4

Age-specific prevalence/105

Khedr et al. Prevalence of Parkinson’s disease in Qena/Egypt

Random sample from one cohort study

Door-to-door survey

Community-based survey in cohort individuals w64 years Hospital-based study

Kimura et al.74/Yamagata, Japan

Seo et al.75/Korea

Seijo-Martinez et al.6/Arosa Island (Spain)

Barbosa et al. /Brazil

Neurological Research

PD: Parkinson’s disease; NA: not available; UKPDS: UK Parkinson’s Disease Society.

Schrag et al.47/London, UK

Bauso et al.76/Buenos Aires City, Argentina

Cross-sectional prevalence survey

Record-based survey (to medical clinics) Hospitals and clinic-based study

Anca et al.73/Israel

7

Type of study

Author/country

Table 6 Continued

753 aged i65 years/15 Screening questionnaire 1,186 aged w 64 years/39 Brain Bank of London diagnostic criteria Not stated of PD Criteria of the UK Parkinson’s Disease 121 608/156 Society Brain Bank and confirming by clinical assessment

Not reported

i2 of resting tremor, bradykinesia, 73 767/180 rigidity and exclusion of other cause all five items: (1) insidious onset after 1 244 040/963 age 20 years. (2) Resting tremor or cogwheel rigidity, with akinesia or smallstep gait. (3) Improvement by antiParkinsonian drugs. (4) No history of drug-induced Parkinsonism. (5) Exclusion of other cause UKPDS Brain Bank Criteria 4700/18 All ages

Diagnostic criteria

128 (all ages)

374 (w18 years) 1990 (i65 years) 3333 (i65 years) 394 (40 years)

118.7 (all ages)

240 (all ages)

Total Crude population/number prevalence/105 (age group) of cases

0–29 years: 0 30–39 years: 8 40–49 years: 12 50–59 years: 109 60–69 years: 342 70–79 years: 691 i80 years: 1265

w40 years: 394

w64 years: 3333

i65 years:1990

w40 years: 330 w60 years: 942 0–29 years: 0.5 30–39 years: 2 40–49 years: 8 50–59 years: 42 60–69 years: 146 70–79 years: 403 w80 years: 341 Not specified

Age-specific prevalence/105

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Comparison of the estimated daily intake in this study with the average daily intake data recommended by the Food and Agricultural Organization/World Health Organization59 showed that none of these values exceed the recommended values. Nevertheless, there is a potential risk with the increased consumption of contaminated milk on human’s health. Priyadarshi et al.60 performed a meta-analysis of studies examining the association between PD and exposure to environmental factors in USA, such as living in a rural area, well water use, farming, and exposure to farm animals, or living on a farm and pesticides. They found that people living in a rural area, drinking well water, farming and who were exposed to pesticides had a higher risk for developing PD. More than half of the cases in Assiut8 were recorded at stage I and II (54.6%) despite the fact that the mean age of the patients (66.94+ 8.45) was higher and the duration of illness (6.17+ 5.9 years) was longer than in the present study where the majority of cases (97%) ranged from 2.5 to 4 HY stage with a short duration of illness (2.75+ 1.3 years) suggesting that these patients had a more rapidly progressive course. About 14.3% of the present cases had mild dementia. This is slightly lower than previously reported (22.3%) by Khedr et al.8 and may be related to the duration of illness and HY staging as described above. The prevalence rate of mild dementia was reported recently among newly diagnosed drug-naive PD patients and PD in early stage 14.8 and 34%, respectively.61,62 This difference in estimation of cognitive impairment in PD may be methodological. The NMS were positive in at least one domain in our PD cases. The highest frequency was found (100%) in the GIT domain followed by urinary and mood/cognition domains in 86 and 80%, respectively, while there were few perceptual problems (11.4%). Our data are partially consistent with reported NMS among PD in Assiut governorate.63 The present study confirms the higher prevalence of PD in our community than that recorded in other Arabic countries and most other countries worldwide. It may be related to environmental risk factors such as air and water pollution and genetic susceptibility. Further longitudinal studies and investigation for risk factors are warranted in future studies.

Disclaimer Statements Contributors Eman M. Khedr contributed to study concept and design, acquisition of data, draft and revision of the report, statistical analysis and interpretation of data. Gharib Fawi, Talal A. Mohammed, and Mohamed A. Abbas contributed to study concept, draft and revision of the report. Noha Abo El-fetoh contributed to study design,

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acquisition of data and statistical analysis. Ghada AL Attar contributed to study design, estimation the sample size and statistical analysis. Ahmed F. Zaki contributed to study design, did the survey, recruited the positive cases, acquisition of data and statistical analysis. Funding No funding has been received on this work. Conflicts of interest The authors report no conflicts of interest in this work. Ethics approval Ethical approval was obtained.

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