61ournal of Neurology, Neurosurgery, and Psychiatry 1997;62:612-616

Psychiatric manifestations of neurocysticercosis:a study of 38 patients from a neurology clinic inBrazil

Orestes Vicente Forlenza, Antonio Helio Guerra Vieira Filho, Jose Paulo Smith Nobrega,Luis dos Ramos Machado, Nelio Garcia de Barros, Candida Helena Pires de Camargo,Maria Fernanda Gouveia da Silva

Department ofPsychiatryO V ForlenzaA H G V Filho

Department ofNeurologyJ P S NobregaL dos Ramos Machado

Department ofRadiologyN G de Barros

Department ofPsychology, Universityof Sao Paulo MedicalSchool, Sao Paulo,BrazilC H P de CamargoM F G da SilvaCorrespondence to:Dr Orestes V Forlenza,Projeto Terceira Idade,Instituto de Psiquiatria,Hospital das Clinicas daFaculdade de Medicina daUniversidade de Sao Paulo,Rua dr Ovidio Pires deCampos S/N, Cep 05403-010 Sa Paulo-SP, Brazil.

Received 11 November 1996and in revised form23 January 1997Accepted 30 January 1997

AbstractObjective-To determine the frequencyand features of psychiatric morbidity in across section of 38 outpatients with neuro-cysticercosis.Methods-Diagnosis of neurocysticerco-sis was established by CT, MRI, and CSFanalysis. Psychiatric diagnoses weremade by using the present state examina-tion and the schedule for affective disor-ders and schizophrenia-lifetime version;cognitive state was assessed by mini men-tal state examination and Strub andBlack's mental status examination.Results-Signs of psychiatric disease andcognitive decline were found in 65-8 and87-5% of the cases respectively. Dep-ression was the most frequent psychiatricdiagnosis (52-6%) and 14-2% of thepatients were psychotic. Active diseaseand intracranial hypertension were asso-ciated with higher psychiatric morbidity,and previous history of mood disorderswas strongly related to current depres-sion. Other variables, such as numberand type of brain lesions, severity of neu-ropsychological deficits, epilepsy, and useof steroids did not correlate with mentaldisturbances in this sample.Conclusions-Psychiatric abnormalities,particularly depression syndromes, arefrequent in patients with neurocysticerco-sis. Although regarded as a rare cause ofdementia, mild cognitive impairmentmay be a much more prevalent neuropsy-chological feature of patients with neuro-cysticercosis. The extent to which organicmechanisms related to brain lesions mayunderlie the mental changes is yetunclear, although the similar sex distrib-ution of patients with and without depres-sion, as well as the above mentionedcorrelations, provide further evidence ofthe part played by organic factors in thecause of these syndromes.

(J Neurol Neurosurg Psychiatry 1997;62:612-616)

Keywords: neurocysticercosis; organic mental disor-ders; depression; psychosis

Neurocysticercosis is the most common para-sitic infection of the human CNS' and is causedby the infection of nerve tissues by the larvalform of the pork tapeworm Taenia solium. Itoccurs endemically in the rural areas of the

developing countries of Asia, Africa, LatinAmerica, and central Europe, where prevalencerates vary from 0-1 to 4-0%.2 8 It may also befound in urban areas of developed countriesamong ethnic subgroups.9 12The two host life cycle of the cestode

involves humans as definitive hosts and swineas intermediate hosts. The adult intestinal formof the parasite is acquired by eating under-cooked pork contaminated with cysticerci,13 14whereas cysticercosis is usually acquired by afecal-oral mechanism-that is, by the ingestionof Taenia solium eggs shed in the faeces of ahuman carrier. Contaminated water and food(especially raw vegetables) are the most com-mon sources of infection.19 16 The digested eggsrelease embryos that actively penetrate themucosa of the upper digestive system and enterthe blood stream. They lodge in muscle, fat,nerve, and eye tissues, and become encysted forseveral years.8 The degeneration of the cysts,which may be spontaneous or induced byantiparasitic drugs, is accompanied by inflam-mation, fibrous encapsulation, and calciumdeposition. Brain pathology is based on severaldifferent mechanisms, depending on the num-ber, type, and location of the cysts, as well asthe host's immune response. 17 19The clinical picture often includes seizures

and hydrocephalus. Mental disturbances aretypically present in the course of the diseaseand were extensively studied by psychiatrists atthe beginning of the century. Mental syn-dromes that could mimic schizophrenia, majoraffective disorders, and dementia have beenpositively reported,20 but few recent studieshave tried to describe the psychopathologyassociated with neurocysticercosis with appro-priate instruments for psychiatric assessment.

MethodsIn the present study, 38 non-selected consecu-tively admitted outpatients from the Section ofNeuroinfectious Diseases of the Hospital dasClinicas University of Sao Paulo (HCF-MUSP) were assessed between January 1993and April 1994. The age range was restricted tobetween 18 and 60 years old. Patients withother neurological or medical conditions thatcould present psychiatric symptoms, as well asthose on drug therapies that could affect themental state (except the ones necessary for thetreatment of epilepsy or intracranial hyperten-sion) were excluded, as well as current alcoholand substance misusers.

Aetiological diagnosis was ascertained by

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positive immunological tests in CSF and tomo-graphic findings suggestive of neurocysticerco-sis (small, multiple, and scattered calcificationsor cystic, contrast enhanced or not, lesionswithin the brain parenchyma).'5' Brain MRIwas performed to provide more sensitive imag-ing of patients with cystic lesions, both for diag-nostic accuracy and detection of parenchymaoedema.21-23

Cases were classified according to the mainsite of lesion location in the CNS (parenchyma,ventricular, subarachnoid, and miscellaneousneurocysticercosis), and also according to dis-ease activity.'8 Cases were considered inactive ifneuroradiological images showed only calcifica-tions or hydrocephalus without cysts, in theabsence of signs of inflammation in the CSFanalysis. Active disease included all cases inwhich cysts (with or without parenchymainflammation) could be found in neuroimagingstudies or cases with inflammatory CSF(increased CSF cells, pleocytosis, and increasedprotein concentrations ) .24

Current mental state was evaluated by thepresent state examination (PSE)25 26 and themini mental state examination (MMSE).'7Previous psychiatric history was assessed withthe schedule for affective disorders and schizo-phrenia-lifetime version (SADS-L).28-31 Abrief neuropsychological test was performedwith Strub and Black's mental status examina-tion (MSE)," which evaluates attention, mem-ory, language (including reading and writing),visuospatial abilities, executive functions(including praxis and motor functions), andhigher cognitive functions. Psychiatric diag-noses were based on the total PSE scores andallocation in the PSE syndromes and classes foreach patient. Patients with suspected psychi-atric disease were submitted to the DSM-III-Rdiagnostic criteria.33 Due to the high prevalenceof illiteracy among the users of the HCFMUSPfacilities, different MMSE cut off points were

used: 13 for the illiterate patients, 18 for thosewith four to eight years of schooling, and 26 forthose with more than eight.34

ResultsAll patients in the study were Brazilian (71%white, 7-9% black, and 21-1 half caste), mostly(60 5%) residents of urban areas (Greater SaoPaulo) and with low educational levels (66%had less than four years of instruction). Theirages ranged from 18 to 59 (mean 36-7), with nosignificant sex differences (47-4% men). There

were four (10-5%) asymptomatic cases.

Epilepsy was the most common presentation,found in 23 patients (60 5%). Six (15-8%) hadhydrocephalus with intracranial hypertension,and five (13-2%) had focal symptoms withoutconsistent evidence of intracranial hyperten-sion. Although there were no patients withsymptoms of meningitis, the CSF analysis of 17patients (45-9%) disclosed signs of inflamma-tion, 11 of whom (29 9%) also had positiveantibody tests. No abnormalities were detectedin the tests of the remaining 20 patients(54 1%) and one patient could not have hisCSF analysed due to severe hydrocephalus.

Active neurocysticercosis was hence diagnosedfor 29 patients (76&3%).

Radiographic data showed that 20 patients(52 6%) had parenchymal cysts or calcificationsonly. Ventricular and cysternal cysts occurredin five (13-2%), and the remainder had sub-arachnoid (5-3%) or miscellaneous lesions(28 9%). Parenchymal lesions were usuallymultiple and scattered, in different stages ofevolution. Only five patients had a single cyst,15 had two to five, and six had more than 20brain lesions (one with more than 300). Bothhemispheres were equally affected, includinglesions in all cortical areas and subcorticalstructures (thalamus and basal ganglia).

Psychiatric diagnosis was based on previous(before this cross section) and current evidenceof mental disease and also on signs of cognitivedecline. Fifteen patients had no evidence ofprevious mental disease and 23 patients(60 5%) had a positive psychiatric historyaccording to the SADS-L interview. Amongthese, 42 research diagnostic criteria (RDC)were met, which indicates that more than onediagnosis was possible for some patients in thislifetime assessment (table 1). Depressive disor-ders (including major, minor, and intermittentdepression) were the most common of thesefindings (15 patients).

Thirteen patients (34 2%) were presumedmentally healthy by the PSE (index of defini-tion < 5), whereas 25 (65 8%) had mild ormoderate psychiatric manifestations compatiblewith at least one psychiatric diagnosis. The PSEsubscores suggested that non-specific neuroticsyndromes (NSNs) were possibly the main psy-chopathological tendency among the casesanalysed, occurring in at least 75% of the testgroup, and achieving here the highest scores.The PSE subscores for specific neurotic syn-dromes (SNRs) and behaviour, speech, andothers (BSOs) occurred in at least 25% of theobservations, and delusions and hallucinations(DAH) in less than 25%. There were nopatients with a typically schizophrenic presenta-tion, although such psychotic symptoms werepresent in four cases (10-5%). Simple depres-sion (SD) and loss of interest and concentration(IC) (23 patients, 60 5%), worry (WO) (22patients, 57-9%), other depressive symptoms(OD) (19 patients, 50%), tension (TE) (18patients, 47A4%), irritability (IT), and specialdepressive features (ED) (17 patients, 44 7%)

Table 1 Frequency ofRDCISADS-L diagnosis in 23patients with neurocysticercosis

RDCISADS-L n (%)

Major depression 12 (52 2)Minor depression 1 (4-3)Intermittent depression 5 (21-7)Mania 1 (4 3)Cyclothimia 1 (4-3)Schizoaffective psychosis 3 (13-0)Panic disorder 3 (13-0)Generalised anxiety disorder 2 (8-7)Simple phobia 3 (13-0)Alcohol related problems 2 (8-7)Abnormal personality traits 2 (8 7)Unstable personality disorder 3 (13-0)Antisocial personality disorder 1 (4-3)Attempted suicide 3 (13-0)

RDC/SADS-L = Research diagnostic criteria schedule foraffective disorders and schizophrenia-lifetime version.

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Table 2 Frequency ofPSE classes (n = 38)

PSE classes n (%)

Retarded depression (R+) 10 (26-3)Neurotic depression (N + /N?) 8 (21-2)Depressive psychosis (D +) 2 (5-3)Schizophrenic psychosis (S + /S?) 4 (10*5)Mania and mixed affective states (M +) 1 (2 6)Non-specific symptoms (X) 6 (15-8)Normal examination (NO) 7 (18 4)

PSE = present state examination.

and loss of energy (LE) (15 patients, 39 5%)were the most common findings in the syn-

drome checklist.Twenty patients (nine men and 11 women;

52 6%) had current signs of depression, if thethree PSE classes retarded depression (R+),neurotic depression (N+, N?) and depressivepsychosis (D+) were combined together (table2). Eleven of those also had evidence of previ-ous depression according to SADS-L and fourpatients had been depressed in the past but notat the time of the evaluation. Sixteen patientsalso met DSM-III-R diagnostic criteria fororganic mood disorder with depressive features(k = 0 4), providing further evidence of relia-bility for the PSE diagnosis of depression.The distribution of MMSE scores ranged

from 12 to 30 (mean 26-9; median 29). Onlyfive patients (three of whom were illiterate)scored less than 20, and the maximum score of30 points was achieved by 10 patients. Whendifferent cut off points were considered,34 onlytwo patients had MMSE performances worse

than expected for their educational levels.However, the neuropsychological assessment of32 patients suggested mild to moderate cogni-tive impairment in 23 (71 -9%) and severe

changes in five (15 6%). Six patients could notbe evaluated because of illiteracy (three), visualdeficits (two), and non-compliance (one).Attention deficits were detected in all thepatients assessed by MSE (59 4% had mild tomoderate and 40-6% severe attention distur-bance). Memory, language, and higher cogni-tive functions were altered in 25, 25, and 28patients respectively, and other deficitsincluded praxis and motor functions (16patients). Reading and writing skills were lessoften affected (nine and two patients respec-tively). However, there was no clear pattern oflocalisation for the neuropsychological dysfunc-tions in the patients of the test group.

Non-parametric statistical procedures were

used to compare the PSE cases of depression(R+, N+, N?, D+) and psychosis (S+, S?, M+)with the non-depressed cases (X, NO).Pearson's x2 test was used for 2 x 2 tableswhenever possible; or alternatively Fisher'sexact test was preferred when dealing withsmall numbers. Relative risk (RR) estimates(odds ratio (OR) with 95% confidence interval(95% CI)) were used to test the associationbetween psychiatric variables (depression, psy-chosis, and cognitive state) and some possiblerisk factors for psychiatric morbidity. Patientsin these groups did not differ significantly on

most demographic characteristics, includingage (F = 1-29, NS), sex (t = 1-59, NS), colourof skin (t = 0-91, NS), marital status (t =

3-22, NS), educational level (t = 0-15, NS),and duration of neurological disease (t = 0 66,NS). No association was found between the useof steroids (11 patients) and current psy-chopathology, both for depression (P = 1 000)and psychosis (P = 0-176), nor betweendepression and severity of cognitive decline (P= 0-569). The occurrence of depression corre-lated positively with disease activity as previ-ously defined (x2 = 4-062, df = 1, P = 0 044;OR = 4-667, 95% CIO,, = 0-995-21-895) andwith the occurrence of intracranial hyperten-sion (P = 0 118; RR = 1-813, 95% CI, =1-306-2 516). Psychosis was also possibly asso-ciated with intracranial hypertension(P = 0065; RR = 5 333, 95% CI, =1-923-14-790) but not with disease activity(P = 0 500). No association was foundbetween the psychiatric manifestations and theoccurrence of epilepsy (P = 0-629). Ven-tricular and cysternal location of cysts also didnot correlate with psychiatric variables (P =0 621) in the test group. Previous history ofdepressive disorders was strongly associatedwith current depression (X2 = 7-620, df = 1,P = 0-006; RR= 2-139, 95% CI,, =1-268-3-607; OR= 14-667, 95% CIo01 =1-590-135 322) and psychosis (P = 0 044; RR= 5-250, 95% CIRR = 1-292-21 339).

DiscussionVery few publications have considered the psy-chiatric manifestations of neurocysticercosis,most of them consisting of anecdotal reports orbrief descriptions of psychiatric cases in neuro-logical studies.7 Clear diagnostic criteria forthe definition of psychiatric cases were notalways used and less severe mental symptomshave probably been overlooked in such studies.Data from psychiatric research in neurocys-ticercosis are basically available from studiesperformed in mental institutions in the first halfof the century, in which detailed clinical andpathological descriptions can be found.38 40 Ourstudy improves on these in some ways: (a) thechoice of a sample of neurological outpatientsmade possible the investigation of psychiatricmorbidity in patients with initial or mild forms ofneurocysticercosis; (b) the use of semistruc-tured interviews and diagnostic criteria pro-vided a more reliable evaluation of current andprevious mental status; (c) cognitive function-ing was assessed by two instruments with differ-ent sensitivity levels; (d) clinical and radio-logical correlations were made, in the firstattempt to identify possible risk factors of psy-chiatric illness associated with this organic dis-ease.The limitation of this study is that no control

groups were used to decide if some of the psy-chopathological findings were greater thanexpected in other groups of non-neurologicalchronically ill patients or in those with a para-sitic infection not involving the CNS. The firstissue has been considered in other studies ofneuropsychiatric conditions (such as stroke andmultiple sclerosis), but no studies haveattempted to describe the psychiatric complica-tions of non-CNS cysticercosis. Such proce-

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dures were beyond the initial scope of this crosssectional descriptive survey, but would defi-nitely be a necessary methodological refinementfor further studies. Also, the present sample waspathologically heterogeneous (lesions of differ-ent types were included) and patients were

assessed only once, hence at different times inthe outcome of a long term disease. Prospectivefollow up of selected patients with cystic lesionsmight detect further abnormalities at the timeof the death of the parasite (treatment inducedor not), which is a situation associated withgreater CNS inflammation and consequentlymore clinical and possibly psychiatric implica-tions.4'Our demographic data (available on request)

are in agreement with the literature.3642-47 Thisstudy confirms that psychiatric manifestationsare frequent in patients with neurocysticercosis.Prevalence rates vary greatly according to theorigin of the patients and diagnostic accu-

2 7 8 18 39 40 45 46 48-58 f8% ofracy. 464-8The finding of 658%omental abnormalities in our cross section is an

estimate of the prevalence of psychiatric mor-

bidity among neurological outpatients withneurocysticercosis. Samples of psychiatric inpa-tients might provide a different profile, withmore severe or even specific forms of mentaldisease. Psychiatric surveys based on patientsfrom mental institutions in the first half of thecentury reported up to 75% of severe mentaldisease in association with neurocysticercosis.Such a high rate might be explained by theduration of the untreated organic disease, as

many of the patients had previous evidence ofneurological syndromes before psychiatricadmission.40 Thus it is possible that mental dis-ease represents one of the consequences of thedeteriorating organic illness, in the absence ofeffective therapeutic strategies for neurocys-

ticercosis at that time.8 Moreover, mentally dis-abled patients may also be at an increased riskof developing neurocysticercosis, for they mightbecome infected from the contact with faecesdue to poor hygiene habits. Although itis a consensus that neurocysticercosis maybe responsible for most of the major psychiatricsyndromes (for example, schizo-phrenic and affective disorders) and demen-tia,7 20 38 394349-51 59-66 a particularly interestingfinding of our study was the non-specific pat-tern of psychiatric morbidity, as shown by thePSE subscores. Very few studies have consid-ered minor psychiatric manifestations or mildcognitive decline in patients with neurocysticer-cosis.35 Possibly such syndromes were underesti-mated by most of the studies, which did not use

instruments sensitive enough for an appropriateassessment, so that only the most dramaticcases of mental or behavioural changes were

usually classified.There was a high proportion of patients with

depression (52 6%), which was the main psy-

chopathological finding. Psychotic disorderswere less frequent than previously reported, butthis might again be explained by the use of a

sample of neurological outpatients, who proba-bly have less severe psychiatric disorders.History of mood disorder was strongly relatedto the occurrence of depression in the patients

from the test group and parallels several otherstudies on the aetiology of organic mood disor-ders. A family history of depression (which waspositive in only three cases in the study) and ahistory of depression before the onset of theorganic disease are regarded as risk factors fordeveloping depression in cerebrovascular dis-ease and multiple sclerosis, by means of agreater biological vulnerability.6768 The lack ofsignificant sex differences among the PSEdepressed patients is used by some authors asevidence of organic aetiology.68 Further evi-dence could be the correlations betweendepression and disease activity and intracranialhypertension, provided we take into accountthat the test group was small in number. Otherauthors have already postulated from descrip-tive studies that intracranial hypertension wasthe syndrome most often related to psychiatricabnormalities in neurocysticercosis.25" Diseaseactivity (which is usually related to a diffuse orlocalised CNS inflammation) is possibly relatedto organic mood disorders, as shown in othermedical and neurological conditions that affectthe CNS, such as systemic lupus erythemato-sus69 and multiple sclerosis,70 but no attempts tocorrelate disease activity with depression havebeen made in patients with neurocysticercosis.Moreover, neurological symptoms in parenchy-mal neurocysticercosis seem to be positivelyrelated to the host's immune response,36 andthe onset of mental abnormalities has also beenreported in the treatment of neurocysticercosiswith antiparasitic drugs,71 both situations asso-ciated with a greater CNS inflammation.

Finally, quite different outputs wereobtained by MSE and MMSE (as expected),even after reallocation of patients according toeducation related MMSE cut off points, whichcould be explained by the greater sensitivity ofthe MSE. Both tests identified patients withsevere cognitive decline, but only MSE wassensitive enough to detect minor neuropsycho-logical abnormalities. Attention deficits werepresent in 100% of the MSE evaluations, prob-ably being influenced by the effect ofantiepileptic drugs (carbamazepine and barbi-turates). Memory was also affected in a highproportion of patients, which is consistent withthe findings of other authors39 50 and reinforcesthe part played by neurocysticercosis in thecause of dementia.20 43 Despite the lack of aproper controlled design for confounding vari-ables (such as illiteracy, high prevalence ofseizures, and use of anticonvulsant medicationand steroids), this is to our knowledge the firstattempt to describe the psychiatric manifesta-tions in patients with neurocysticercosis byusing standardised psychiatric instruments, aswell as the first study to assess some possiblerisk factors for psychiatric morbidity associatedwith this cerebral disease. None the less, suchfindings clearly indicate the need for furtherexploration in this area.

This work was submitted in part to the University of Sao PauloMedical School as the MPhil thesis of OVF.

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