Occupation, Education, And Parkinson's Disease- A Case-control Study in an Italian Population

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Movem en i DisordersVol. 1 1 , N o. 2 , 1996, pp . 201-2060 996 Movement Disorder Society

Occupation, Education, and Parkinsons Disease: ACase-Control Study in an Italian PopulationWalter A . Rocca , *Dallas W . Anderson, tFrancesca Meneghini, tFrancesco Grigoletto,

SLetterio Morgante, SArturo Reggio, IlGiovanni Savetti eri, a nd SRaoul Di PerriDepartment of H ea l t h S c i en ces R es ea r ch , M a yo C l in ic m d M a yo F o u n d a t io n , R o ch es t e r, M i n n es ot a , U . S . A . ;*Biometry and Field Stud ies Branch, Na t ional inst i tute of Neurological Disorders and Stroke, Bethesda, Maryland,U . S . A . ; i n s t i t u f e of Hygiene, Universi ty of Padu a , Paduai I ta ly; $Depar tment of Neusology, Universi ty of Mess ina ,Mes sina, I taly; 9L)epartment of Neurology, Universi ty of Catun ia , Ca tan ia , I ta ly; and \ Depar tmentof Neuro logy ,Universi ty of Palermo, P a lesmo, I ta ly

Summary: Current epidemiologic data on the associationbetween occupational exposures and Parkinsons disease(PD) are inconsistent. In a case-control study, we inves-tigated the associations between occupation and PD andbetween education and PD. The cases (n = 62) werethose identified in a prevalence survey (door-to-door,two-phase) of three Sicilian municipalities, as of Novem-ber 1 , 1987. We then randomly selected from the generalpopulation two controls for each case, matched for age(21year), sex, and municipality (n = 124). Informationon current and past occupations and education for cases

and controls was obtained during the survey. Subjectswho worked for most of their lives as farmers were not atincreased risk of PD (O R = 0 . 6 ; 95 % CI = 0.3-1.3).Neither were subjects who worked for most of their livesin other occupations (e.g., housewives, fishermen, fac-tory workers, salesmen, craftsmen, clerks). PD was notassociated with low education. Our findings suggest thatfarming, as a broad occupational category, does not playa major role in the causation of PD. Key Words: Par-kinsons disease-Risk factors-Case-control studies-Occupation-Education.

A prevalence survey of Parkinsons disease (PD)was conducted in three municipalities of Sicily, It-aly. The field work involved door-to-door screeningof eligible subjects and neurologic evaluations ofthose who had screened positive (1). Only threeother similar surveys have been fully reported thusfar: in Copiah County, Mississippi (2), in six citiesof the Peoples Republic of China (3), and in Parsicommunities of Bombay, India (4).

The age-specific prevalence figures in the Siciliansurvey were greater than those found in these othersurveys (1). It is possible that Sicily is a high-riskarea for PD, although methodologic influences(e.g., case finding, diagnostic criteria) might be apartial explanation for the greater prevalence fig-

__ _Accepted September 12 , 1995.Address correspondence and reprint requests to Dr. W . A.Rocca at Department of Health Sciences Research, Mayo Clinic,200 First Street S W , Rochester, M N 55905, U 5.A.

ures (1). Because of budget constraints, we wereunable to undertake an extensive case-control studyin conjunction with the Sicilian survey or followingit. Nevertheless, because we had collected sociode-mographic information for essentially the entirepopulation of the three municipalities, we pro-ceeded to investigate the relationship between oc-cupation and education and PD. This research is thefocus of the present article.

An association between farming and farming-related exposures and PD was shown by three stud-ies (5-7), but not confirmed in five others (8-12). Toour knowledge, there have been no published re-ports linking education and PD. However, we de-cided to investigate a possible link because of anal-ogies between PD and Alzheimers disease (13,14).Several studies recently reviewed by Mortimer andGraves (15) have reported a decreased risk of Alz-heimers disease with increased education. By con-trast, some other studies did not confirm the asso-ciation (16,17).

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202 W . A . R O C C A ET AL.METHODS

CasesWe included all the cases of PD identified during

the aforementioned Sicilian survey. That survey in-vestigated the prevalence of PD and other types ofparkinsonism among subjects who resided as of No-vember I , 1987, in any of three municipalities: Ri-posto in Catania Province, Santa Teresa di Riva inMessina Province, and Terrasini in Palermo Prov-ince. All subjects living in households and thoseinstitutionalized were included. Cases were ascer-tained through a two-phase approach. In the firstphase, medically trained interviewers administereda brief screening instrument that included symptomquestions and physical tests. In the second phase,study neurologists used specified diagnostic criteriato evaluate those subjects who screened positive.Diagnoses were reviewed for each municipality bythe local senior neurologist; in addition, they wereadjudicated by a study panel to increase homoge-neity across the three municipalities. For subjectswho could not be clinically examined, relevantmedical information was sought from close relativesand from their general practitioners (1). Further de-tails regarding the Sicilian survey were reportedelsewhere (1,18-20).A diagnosis of PD required the presence of atleast two cardinal signs (resting tremor, rigidity,bradykinesia, impaired postural reflexes) in a sub-ject not receiving antiparkinsonian therapy or atleast one sign in a patient specifically treated. PD,or idiopathic parkinsonism, was defined by exclud-ing other causes of parkinsonism through medicalhistory information and direct patient examination.Specified diagnostic criteria were used for drug-induced parkinsonism, parkinsonism in vasculardisease, and postencephalitic parkinsonism; otherless common types of parkinsonism were definedby routine clinical diagnosis without specified cri-teria (1). Cases of parkinsonism for which the clin-ical information was insufficient to reach an etio-logic classification were also excluded from thisstudy ( I ) .

ControlsTwo population controls were matched by age

( & I year), sex, and municipality to each case in-cluded in the study. The controls were selectedamong all residents included in the Sicilian surveyand found to be free of parkinsonism, as of Novem-ber 1 , 1987. No other exclusion or inclusion criteria

were applied; in particular, the presence of neuro-logic diseases other than parkinsonism was not anexclusion criterion. When more than two potentialcontrols were available for a given case, two ofthem were selected using a table of random num-bers.

Data CollectionDuring the Sicilian survey, the interviewers who

administered the screening instrument (see above)also gathered information about occupation and ed-ucation. This was accomplished for cases and con-trols with a structured questionnaire. Subjects wereasked about all their current and past occupations;because most of them had held only one occupa-tion, a principal lifetime occupation was usuallystraightforward to derive. Housewives of farmerswere classified as farmers if they had regularly par-ticipated in farming activities. Subjects were askedwhether they were literate; they were also asked togive the number of years that they completed inschool. If a subject was unavailable or judged un-able to respond, the questions were put to a proxyrespondent (closest available relative of the subject)(20) .

Data AnalysisConsistent with the study design, matched triplet

analyses were used, and the odds ratio served toestimate the relative risk (21) . For each study vari-able, we computed a maximum likelihood estimateof the relative risk, an approximate 95% confidenceinterval, and a p value (two-tailed test, alpha =0.05) (21,22). For education, we also investigateddose-effect contrasts using conditional logistic re-gression for matched sets (21). Education was cat-egorized in three classes, and 3 5 years of educa-tion served as the reference.

RESULTSOf the 63 prevalent cases of PD in the three mu-

nicipalities surveyed, 62 were included in the cur-rent study. The remaining case of PD was excludedbecause no suitable controls were available formatching. Although our diagnostic criteria includedpatients with at least one sign of parkinsonism whenspecifically treated, all of the 62 cases of PD in-cluded in this study happened to have two or morecardinal signs. More extensive details about theclinical characteristics of our case series were re-ported elsewhere (1). Table 1shows the distributionof cases by age and sex. By virtue of the matching,

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O C C U P A T IO N , E D U C A T IO N , A N D P A R K IN SO N ' S D ISE A SE 203TABLE 1. Age and sex distribution of the 62 cases ofParkinson's disease"

~ ~

Women Men TotalAg e(years) No. Percentage No. Percentage No. Percentage

At onset of Parkinson's disease4049 1 2.9 2 7.4 3 4.850-59 3 8.6 3 11 . 1 6 9.760-59 17 48.6 9 33.3 26 41.970-79 11 31.4 12 44.4 23 37.180-89 3 8.6 1 3.7 4 6.5Total 35 100.0 27 100.0 62 100.050-59 1 2.9 2 7.4 3 4.8m 9 7 20.0 6 22.2 13 21 o70-79 19 54.3 12 44.4 31 50.08&89 8 22.9 7 25.9 15 24.2Total 35 100.0 27 100.0 62 100.0

At the time of the studyb

a One case of Parkinson's disease (a woman 93 years old on the prev-alence day) was excluded from the case-control study because no suitablecontrols were available.Age on November 1, 1987.

the 124 population controls had a similar age andsex distribution. The information regarding occupa-tion and education was obtained for all cases andcontrols; therefore, all triplets (case, control 1 , con-trol 2 ) were complete for analysis. However, proxy

respondents were used for one case of PD (subjectincapacitated) and six controls (three subjects inca-pacitated, one refused, two unreachable). Theproxy respondents were one offspring for the case,and three offspring, one spouse, one sibling, andone niece or nephew for the controls.

Table 2 shows the case-control results for princi-pal lifetime occupation and education; none werestatistically significant. We note two suggestivefindings-that farmers had a decreased risk and il-literates an increased risk for PD. Because of thefinding for illiterates and the postulated analogywith Alzheimer's disease, we also conducted dose-effect analyses contrasting multiple levels of educa-tion. These analyses failed to show a more definiteassociation between education and PD.

DISCUSSIONTable 3 lists the case-control studies that haveinvestigated associations between PD and farming

practices. In terms of case finding, our study isunique because we included all prevalent cases ofPD from a door-to-door survey (the aforementionedSicilian survey). That survey had achieved high re-

TABLE 2. Association between Parkinson's disease and categories of occupation and education (6 2 cases and124 controls)Outcome among case-control triplets(case, control 1, control 2)

++- -+ - Odds ratioFactor + - - + - + +++ - - - + -++ (95%CI) P_

Principal lifetime occupation"Farmer I 3 1 30 16 5 0.6 0.34Fisherman 2 2 0 55 3 0 1.9 0.69Factory worker 6 0 0 48 8 0 1.5 0.64Craftsman 4 0 0 49 9 0 0.9 0.92Salesman 3 0 0 5 3 6 0 I .o 0.72Clerk 4 0 0 48 10 0 0.8 0.92Housewife 3 9 10 29 8 3 1 . 1 0.94Other I I 0 43 I 1 0 1.4 0.69

(1 = yes; 0 = no) (0.3-1.3)(1 = yes; 0 = no)( 1 = yes; 0 = no)( I = yes; 0 = no)

(0.4-10.6)(0.54.3)(0.3-2.5)

( 1 = yes; 0 = no)( 1 = yes; 0 = no)( 1 = yes; 0 = no)

(0.3-3.5)(0.3-2.2)

(0.5-2.6)(1 = yes; 0 = no) (0.5-3.3)Educational levelbIlliterate 9 6 0 35 12 0 1.9 0.15

Under 5th grade 7 19 10 6 1 1 9 1 . 1 0.79(1 = illiterate; 0 = all other) (0.94.4)(0.6-2.2)1 = 4 t h grade; 0 = all other)~

* Each occupation was contrasted to all others using dichotomous contrasts.We also investigated dose-effect contrasts using conditional logistic regression for matched sets. Using 3 5 years of education asreference (O R = l . O ) , we obtained: OR = 1.8 (CI: 0.7-4.8) for illiterates and OR = 0.9 (CI: 0.5-1.8) for subjects with


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204 W. A . ROCCA ET A L .TABLE 3 . Comparison with previous ca se-control studies of the association betw een farming pra ctices undParkinson's disease

Author, year(country) Type a ndno . of cases Type and Odds Comments 'n dno . of contro ls ratioY definition.,Tanner et al., 1989(China)Ho et al., 1989

(Hong Kong)Koller et al., 1990(Kansas , U.S.A.)Globe et al. , 1990(New Jersey, U.S.A.)Hertzman et al. , 1990(British Columbia, Canada)Semchuk e t a l . , 1992(Alberta, Canada)Hubble et al., 1993(Kansas , U.S.A.)Butterfield et al. , 1993Present study(Oregon and Washington, U.S .A.)(Sicily, Italy)

Hospital outpatients,Hospital and nursing homes,Hospital outpatients,Hospital, n = 106General practice patients,n = 57Case register,n = 130Hospital outpatients,n = 63

n = 100n = 35n = 150

Hospital outpatients,Prevalent cases;n = 63door- to-door survey.n = 62

Hospital outpatients,n = 200Hospital and nursinghomes, n = 105Hospital outpatients,n = 150Spouses , n = 106

Population members,n = 122Population members,n = 260Hospital outpatients orvolunteers, n = 75Hospital outpatients orvolunteers, n = 75Population members,n = 124

0.65.2"1.31.33.4"1.9"-

0.4"0. 6

Inverse direction fo: villageFarming for >20 yearsEv er farmed as an crccupationExposure to farm animalsEver worked in an orchardAgricultural workFarming as an occupation wasnot different in c'tses andcontrolsInverse direction. ever livedor worke d on a fx mInverse direction, farming arprincipal lifetimeoccupation

residenceb

Statistically significant.Also inverse direction for pig, chicken, or ot her livestock raising. and for wheat, co rn, or soybean growing; no association with fruit or ricse growing.

sponse rates: 92% of eligible persons were directlyor indirectly screened, and 99% of those whoscreened positive were examined or indirectly eval-uated (1). Also, in a small investigation of validity,the screening instrument for PD was found to beboth sensitive and specific (19). Five of the ninestudies in Table 3 were based on hospital series ofboth cases and controls (5,8,9,11,12). One studywas based on a hospital series of cases, with spousecontrols (10). Two studies obtained cases throughgeneral practice lists or a morbidity register, withpopulation controls (6,7). These two studies aresomewhat more comparable to ours and can be con-sidered population-based rather than hospital-based.

Our odds ratio (O R = 0.6) suggested, if anything,a negative association between PD and farming asan occupation, but that finding is not unprecedented(8,12). To interpret this odds ratio, it is important tokeep in mind that (a) we considered only the prin-cipal lifetime occupation rather than all occupationsheld; (b) we did not obtain data on duration orchronological sequence of occupations ; and (c) wedid not investigate specific tasks or occupationalexposures. Because we restricted our attention tobroad categories of occupation, we were unable todistinguish between subcategories of farmers whoraised particular crops or used specific pesticides orherbicides. It is possible, therefore, that althoughfarmers in general were not at increased risk for PD,

those who worked with specific toxins were at in-creased risk.By means of the Sicilian survey, we gained ac-cess to many previously undiagnosed cases of PDthat never would have come to light if case findinghad been restricted to health-care providers such ashospitals, clinics, or physicians. The characteristicsof the 21 (34%) cases of PD diagnosed during theSicilian survey (by the survey team) differed in sev-eral ways from the characteristics of the 41 (66%)cases of PD diagnosed before the survey. ]Dropor-tionately , or the newly diagnosed cases, there weremore women, more subjects with later onset, morewith shorter duration of symptoms, fewer withtremor, and more with impaired postural reflexes.The proportion of newly diagnosed cases increasedwith advancing age for women but not for men (1).We emphasize that all newly diagnosed cases ofPD, as well as all those previously diagnosed, hap-pened to have two or more cardinal signs of parkin-sonism.The previously undiagnosed cases of PD would,of course, be missing from any health-care providerseries. The differences between previously undiag-nosed and previously diagnosed cases of PD maycreate an important referral (or admission rate) biasin studies based on hospital series and, to a lesserdegree, in studies based on series from other health-care providers (23). Occupation, education, andother socioeconomic factors may influence the like-

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O C C U P A T I O N , E D U C A T I O N , A N D P A R K I N S O N S D I SE A SE 205lihood and the timing of a case coming to medicalattention. The potential impact of hospital referralbias in epidemiologic studies was recently illus-trated for Alzheimers disease in a study conductedin Rochester, Minnesota (24). The study showedthat population-based cases of Alzheimers diseasediffer from hospital referral cases in their distribu-tion by sex, age at onset of symptoms, education,occupation, living arrangement, and marital status(24). By analogy, a case-control study of PD basedon a hospital series may yield spurious findings re-garding occupation and education (i.e., creating anartifactual association or concealing a real one).

Although our study design is strong against thereferral bias, it is weak against a second type ofselection bias, the prevalence-incidence (or Ney-man) bias (23), because we used prevalent cases ofPD instead of incident cases. If, for example, farm-ing was an important negative prognostic factor forPD, we could have underrepresented in our casepool those farmers who developed PD and diedshortly thereafter. This bias would obscure the as-sociation between PD and farming. A similar biascould obscure the association between PD and ed-ucation.

The information on occupation and education wasobtained by trained interviewers at the time of screen-ing and, therefore, before the diagnosis of PD wasestablished or excluded in a subject. We attempted tolimit the risk of exposure suspicion bias (23) by keep-ing the study hypotheses from the interviewers. Inthis endeavor, the scope of the Sicilian survey workedin our favor because exposure data and screening in-formation for several diseases were collected at thesame time. Nevertheless, the interviewers were allphysicians, and it is difficult to know the extent towhich they linked any specific question to any spe-cific disease. With regard to the subjects with PD, wecannot rule out a recall bias (23) in those (66%) diag-nosed before the Sicilian survey.

For cases and controls, direct interviews wereusually used to elicit information about occupationand education. The few indirect interviews withproxy respondents were unlikely to introduce anyasymmetry into the data collection, because theywere a small percentage (4%) of all interviews andbecause proxy respondents were found in otherstudies to be reliable for basic questions such asthose regarding occupation and education (25,26) .

As our sample size was relatively small, we mayhave failed to detect associations between PD andvarious categories of occupation or education for

lack of statistical power. To increase the power ofthe tests conducted in the study, we used a matcheddesign with two controls for each case. For factorsoccurring in 15-60% of the controls (farmer, house-wife, illiterate,


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W . A . R O C C A ET A L .F i n a l l y , we n o t e that t h e a b s e n c e of l i n k s b e -tween PD a n d o c c u p a t i o n and b e t w e e n PD a n d e d -ucation is consistent since occupation and e d u c a -

t ion t end to b e related.

11 . Hubble JP, Cao T, Hassane in RES, Neuberger JS, Kol le rWC. Risk factors for Parkinsons disease. Neurology 1993;43: 1693-1 697.12. Butterfield PG, Valanis BG, Spen cer PS, Lindernan CA,Nutt JG. Environmental anteceden ts of young-onse Parkin-sons disease. Neurology 1993;43:1150-1 158.Acknowledgment: This research was presented in part

at the 45th meeting of the Am erican Academy of Neurol-ogy, New Yo rk, April 1993. This investigation was finan-cially supporte d by the A ssessorato alla Sanita della Re-gione Sicilia (grant no . 58iP) and by Fidia Re search L ab-orator ies , Abano Terme, I ta ly . We thank the manypersons of Riposto, Santa Teresa di Riva, and Terrasiniwho provided assistance during the study. In addition, wethank the field workers: Rita Bella, Biagio Castiglione,Maria Giuseppa Castiglione, Maria Angela C oraci, Vale-ria Costa, Antonio Crisafulli, Antonella DArpa, PietroDe Domenico, Domenico De S h o n e , Giuseppe Di Ste-fano, Alfio Mauro Finocchiaro, Francesco Patti , RosaMaria Ricci, Conc etta Rue llo, Giuseppe Salemi, RaffaellaSan tange lo , V incenzo Sapor i to , Car rne lo S ta ropo l i ,Giuseppe Troilo, and Angelo Xerra. W e are also gratefulto Karen Tennison for typing the manuscript.

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Occupation, Education, And Parkinson's Disease- A Case-control Study in an Italian Population