Bancroftian filariasis in two urban areas of Recife, Brazil: pre-control observations on infection and disease

TRANSACTIONS OF ~‘HE ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (1995) 89, 373-377 373

Bancroftian filariasis in two urban areas of Recife, Brazil: pre-control observations on infection and disease

M. F. M. Albuquerque’*, M. C. Marzochi2, P. C. Sabroza3, M. C. Bragal, T. Padilhal, M. C. M. Silva’, M. R. F. Silval, H. C. Schindler’, M. A. Maciell, W. Souza and A. F. Furtado 1 ‘Centro de Pesquisas Aggeu MagalhBes, Funda@o Oswald0 Cruz, e Departamento de Medicina Clinica, Universidade Federal de Pernambuco, Avenida Moraes Rego sin CEP 50670420, Recife, Brazil; 2Departamento de Cikkcias Biol6gicas and 3Nticleo de DoenGas Endkicas, Escola National de Satide Pziblica, Funda@o Oswaldo Cruz, Avenida Leopold0 BulhGes no. 1480, CEP 21041-210, Rio deganeiro, Brazil

Abstract Bancroftian filariasis is a major public health problem in the city of Recife in north-eastern Brazil. In some of its urban areas microfilaraemia prevalence reaches 14%. This study describes epidemiological characteristics, infection and disease, in 2 urban areas, Coque and Mustardinha, before control measures were ap- plied. The parasitological survey was performed by a ‘door-to-door’ census covering 5563 subjects, aged between 5 and 65 years. Microfilaraemia was detected by the thick drop technique, using 45 PL of peripheral blood collected between 20:00 and 24:O0. In both areas the prevalence of microfilaraemia was lo%, and males had higher prevalences of infection and disease than females. The prevalence of microfilaraemia was higher in the 15-24 and 25-34 years age groups in both sexes. Most microfilaria (mf) carriers (72.1% in Coque and 79.7% in Mustadrinha) had mf densities < 100160 PL of blood. Females of reproductive age had significantly lower mf densities than males. The overall disease prevalence in both areas was 6.3%. Amongst the subjects who presented with chronic disease 15.7% were microfilaraemic. Chronic disease prevalence in- creased from 1.4% in the S-14 years age group to 11.3% in the oldest age group. The most frequent clinical manifestation was hydrocele (5.4%), followed by lymphoedema (1.8%). The epidemiological pattern of filariasis in the populations studied was marked by high prevalence of microfilaraemia, low mf density, and relatively low prevalence of filarial disease considering the level of endemicity.

Keywords: filariasis, Wuchereria bancrofti, epidemiology, Brazil

Introduction About 78 million people in the world are infected by

lymphatic filariasis (WHO, 1992), of whom 92.6% are estimated to be infected by Wuchereria bancrofti, an important public health problem in urban areas. This fact is probably associated with the disordered settlement of populations in the cities of developing countries (MOTT et al., 1990).

_ -

Bancroftian filariasis is characterized by a wide range of host responses to filarial infection. In an endemic area one can find some asymptomatic microfilaremic individuals, others symptomatic and amicrofilaraemic, and a few with both microfilaraemia and disease. There is a wide spectrum of clinical manifestations. The most important are related to lymphatic damage, acute lymphatic inflammation and chronic lymphatic pathology (OT- TESEN, 1992). Other manifestations are very much less common, such as tropical pulmonary eosinophilia, re- sulting from hyper-responsiveness of the human host against the microfilariae (mf) (PARTONO, 1987).

In Brazil, Recife is the most important endemic focus of W. bancrofti, and Culex quinquefasciatus is the vector. Between 1954 and 1983, the prevalence of microfilaraemia in this city decreased from 6.9% to 1.5% (MINISTY& RIO DA SACJDE; 1983). The following decade was characterized bv a rise in orevalence to 3.5% in 1991 ~MINIST&O DA SA~DE: 1991). Some clusters in the urban area-generally in slums-showed prevalence levels close to 15% (WHO, 1992).

A programme designed to compare the efficacy of di- ethylcarbamazine (DEC) chemotherapy with and without vector control has been developed in 2 urban areas of Re- cife (Coque and Mustardinha) by the Aggeu MagalhIes Research CentreiOswaldo Cruz Foundation. Before in- itiating control, a parasitological survey and very careful clinical examinations were undertaken. This is important because previous surveys have focused primarily on microfilaraemia prevalence, although the most obvious clinical manifestation. elenhantiasis. has also been reported (AZEV~~DO &’ DO~BIN, 1952; RACHOU et al., 19561. Studies of filarial morbiditv in Recife have been performed in response to demand: or based on patients referred to specialized out-patient clinics (DREYER et al.,

1989; DREYER & MEDEIROS, 1990), rather than in the context of population surveys.

This paper deals with the epidemiological aspects of filariasis, both infection and disease, in Coque and Mus- tardinha, before the application of control measures. The data will allow the evaluation of the efficacy of control in- terventions and will contribute to elucidating the interac- tions between infection and clinical disease in human populations.

Materials and Methods Selected areas and population studied

Recife, capital of the State of Pernambuco, has an area of 219 km2 and, in 1991, 1 290 149 inhabitants. Up to 60% of the population have a very low income and most live in slum areas (ROCHA & VILLELA 1990; FIBGE, 1992), where households are not connected to an under- ground piped sewerage system. In order to evaluate filariasis control procedures, 2 districts were selected inside the urban area, Coque (area 1) and Mustardinha (area 2); both are slum areas, 6 km apart, with similar environ- mental conditions and levels of microfilaraemia prevalence.

Before performing the clinical and parasitological surveys, the selected areas were mapped and social workers visited all the houses, in order to inform and explain, in detail, the purposes of the research, and to obtain the support of the population. Every person, from 5 to 65 years of age, was defined as a subject to be offered an examination and treatment with DEC.

Microfilaraemia prevalence and density The survey was performed by a ‘door-to-door’ census

between December 1990 and Iulv 1991. Microfilaraemia was detected by the thick droi technique, using 45 E(L of peripheral blood, collected between 20:00 and 24:O0. A second blood sample was taken from subjects with microfilaraemia and 60 PL used to prepare films in order to measure mf density.

Filarial morbidity survey All the subjects were invited to the out-patient units,

one in each selected area, on the day following blood col- lection. Medical staff from the Aggeu Magalhges Re- *Author for correspondence.

374

search Centre interviewed and examined the subjects for signs and/or symptoms of lymphatic lilariasis. During the last month of the research, household visits were made in order to examine the people who did not come to the out-patient units.

Lymphatic filariasis was classified into acute or chronic manifestations. Acute disease was defined as one or 2 fever episodes (whether or not followed by head- ache, nausea and vomiting) and by localized disease (pain, heat, lymphangitis or adenolymphangitis of arms and legs, male genitalia or breasts) for at least 3 d. Chronic disease was identified according to the World Health Organization criteria for lymphoedema, elephantiasis, hydrocele or chyluria (WHO, 1984, 1992).

Isolated cases of adenitis were not included in the filarial disease prevalence calculations because they might have been associated with other diseases. Respiratory disease that could suggest tropical pulmonary eosinophilia, and haematuria without signs or clinical symptoms of other disease, were also excluded.

Data analysis Data were analysed using the EpiInfo program, ver-

sion 5.1. Stratified analyses available in the program

were used to verify the differences between proportions and prevalence ratio by sex and age groups. For some results both the crude and the adjusted prevalence ratio are presented.

Results Microfilaraemia prevalence

There were 3213 residents in area 1, of whom 2702 were aged between 5 and 65 years. Of these, 2321 (85.9%) were examined and 248 (10.7%) were found to be microfilaraemic. Of the 3369 residents in area 2,2873 were aged between 5 and 65 years; 2276 (79.2%) of the latter were examined and 212 (9.3%) were microfilaraemic.

Microfilaraemia prevalence according to age and sex In area 1, the prevalence of microfilaraemia was 7.6%

in the 5-14 years old group and rose to a plateau of 13.8% and 13.3% in the 15-24 and 25-34 years old groups respectively. Prevalence fell to 12.2% in the 35- 44 years age group and 7.3% in the 45-54 years group, after which it rose again to 10.7% in the 55-65 years group (x2= 19.46; P~O.001).

In area 2, the prevalence of microfilaraemia was 5.3%

Table 1. Prevalence of W. bancrofiimicrofilaraemia by sex and age groups in Coque (area l), Recife, Brazil in 1991

Age groups (years)

Prevalence of microfilaraemia Males Females

No. No. No. No. examined infected examined infected

95% Prevalence Confidence

ratio interval P

5-14 15-24

$1;:

$1;; Total

398

fE 98

;: 1056

Table 2. Prevalence of in 1991

149 (14.1%)

434

Ii; 131 3 (2.3%) 101

12::

0.93 1.61 1.86

11.14 3.21 2.82 1.80

0.58-1.50 1.05-2.47 1.13-3.06 3.46-35.84 1~01-10~21 1.00-7.95 1.42-2.29

0.765

K! <O.OOl

0.037 0.040

<O.OOl

W. bancrofti microfilaraemia by sex and age groups in Mustardinha (area 2), Recife, Brazil

Prevalence of microfilaraemia Males Females 95%

$e;E)ouPs No. No. No. No. Prevalence Confidence examined infected examined infected ratio interval P

5-14 333 15-24 2: ;f) ($:g] 326 25-34 174 29 (16.7%) 235

153

12 1249

1.21

::g 2.07

2: 1192

0.63-2.33 1.53-3.96 1.10-3.16 1.01-4.26 1.35-12.23 0.242.33 1.47-2.50

0.570 <O.OOl

0.018

EE 0618

<O.OOl

TmaFtk13. Clinical manifestations of bancroftian filariasis in Coque (area 1) and Mustardinha (area 2), Recife, Brazil

Clinical manifestations

Coque Mustardinha Total No. No. No. No. No. No.

examined affected examined affected examined affected

Acute disease Adenolymphangitis 1842

C~~!Jfdf$P$;yhltl~ 796

Lymphoedema 1842 Elephantiasis 1842 Hydrocele 796 Chyluria 1842

Other manifestationsa Haeqaturia 1842 TPE Adenitis E

aExcluded from calculation of disease bTropical pulmonary eosinophilia.

11 (0.6%) 24 (3.0%)

prevalence.

1014 381

9 (0.9%) 11 (2.9%)

1014 21 (2.1%)

%‘: 2; (&g i 1014 0

1014 2 1014

(0.2%)

1014 117 (K~ I

2856 1177

2856

:F? 2856

2856 2856 2856

375

at 5-14 years, increasing to 11.5% and 12.2% in the 15- 24 and 25-34 years age groups and decreasing to 10.5%, 9.0% and 7.9% in the 3 older groups respectively (x2=20.76;P<O.O01).

When the prevalences in males and females by age groups were compared in both areas, there was no difference related to sex in children aged 5-14 years but prevalence was significantly greater in males than in females aged 15-54 years. Females in area 2, aged 55-65 years, had a higher frequency of microfilaraemia than males, although the difference was not statistically significant (area 1: prevalence ratio [PR]= 1.80, summarized Mantel-Haneszelx2=23.51, P<O.OOl; area 2: PR=1.92, summarized Mantel-Haenszel x2=23.77, P<O.OOl) (see Tables 1 and 2).

Microfilarial density The distribution curve of mf density was similar in

both areas. Most of the infected subjects (72.1% in area 1 and 79.7% in area 2) had ~100 mfi60 uL (Fig. 1). Over-

01 0 100 200 300 400 500 600 700

Densities

Fig. 1, Density of microfilaraemia (microfilariaei60 pL) due to W. ban- crofri in Coque (A) and Mustardinha (*), Recife, Brazil in 1991.

all, the mf density was lower in females, and the difference was statistically significant in the 15-44 years age group (Kruskal-Wallis test based on ranks, P<O.O5). The median values were 33 mfi60 uL for females and 5 1 mfi60 uL for males, considering both areas together.

Clinical survey Of 4597 subjects enrolled in the parasitological survey,

2863 (62.3%) were clinically examined. We compared the parasitologically and clinically surveyed populations in relation to characteristics such as sex, age and microfilaraemia, and found no difference associated with age class or prevalence of microfilaraemia. In relation to sex, we observed a significant difference in area 2 only, where the percentage of males was 45.1% in the parasitological survey and 38.8% in the clinical survey.

The overall prevalence of acute and chronic disease was 6.3%. The prevalence of disease in microfilaraemic subjects (9.4%) was significantly higher than in amicrofilaraemic persons (5.7%; P=O.OlO). When analysed by acute and chronic categories, the higher prevalence amongst the microfilaraemic subjects was statistically significant only for acute disease (Mantel-Haenszel x*=4.79, P=O.O20). Chronic disease was more frequent than acute in both areas.

Among the acute manifestations, epididymo-orchitis was more frequent than adenolymphangitis in both areas (Table 3). Adenolymphangitic episodes were more frequent in females. About 30% of the subjects with epididymo-orchitis, and 5% of those who gave a history of adenolymphangitis, were mf carriers.

The most frequent chronic manifestation was hydrocele, followed by lymphoedema (Table 3). Lym-

phoedema and elephantiasis (80% located in lower limbs) were more frequent in females, and most of the subjects (98% of those with lymphoedema and 89% of those with elephantiasis) were amicrofilaraemic; 26% of the subjects with hydrocele were mf carriers.

Prevalence of acute and chronic filarial disease according to age and sex

Prevalence of acute and chronic disease was higher in males than in females in both areas (PR=3.08, summarized Mantel-Haenszel x2= 15.31, lVO.001, and PR=2.30, summarized Mantel-Haenszel x2=21.16, P<O.OOl, respectively).

Considering both areas, the prevalence of acute disease was 3.8% in the 25-34 years age group, and decreased to <1.5% in the older groups (x*=24.5!, P<O.OOl) (Fig. 2). The prevalence of chronic disease, m both areas, was 1.4% in the 5-14 years age group rising to 11.3% m the 55-65 age group (x2=56.24, P<O.OOl) (Fig. 2).

5-14 15.24 25.34 35.44 45-M 55.65

Age group (years)

Fig. 2. Prevalence of acute (+) and chronic (m) disease caused by W. bancroft according to age in Coque and Mustardinha, Recife, Brazil in 1991.

Discussion The prevalence of microfilaraemia in our sample,

(10.7% in area 1 and 9.3% in area 2) indicates a high level of endemic tilariasis, according to the World Health Or- ganization (OMS, 1988). Considering that the thick drop technique based on 45 yL of peripheral blood is not highly sensitive (SOUTHGATE, 1974), these prevalences are likely to be underestimates.

The age dependency of microfilaraemia prevalence was in accordance with what has been described in the lit- erature, a low frequency of cases in the first 10 years of life followed by a consistent increase to a plateau in the second and third decades and then a gradual decline (SOUTHGATE, 1974; RAJAGOPALAN et al., 1989). The highest prevalence of microfilaraemia occurred in the 15- 24 and 25-34 age groups in areas 1 and 2 respectively, suggesting an intense level of transmission.

The sex-specific microfilaraemia prevalence pattern which we found agrees with previous reports; there was a significantly higher prevalence in males than in females >I5 years old (RAJAGOPALAN et al., 1989; WHO, 1992) and females in the 15 to 44 years age classes had mf densities significantly lower than those seen in males (P=O.O16).

In a recent review, BRABIN (1990) reported that, in 43 of 53 reports from several continents, values for prevalence of infection were lower in females than males and prevalence was consistently lower in females during their reproductive years. The same review also pointed out that mf density was reduced in females between 20 and 39 years of age, in a variety of exposure conditions. The difficulty in detecting low mf densities with the diagnos- tic procedures frequently used in population surveys could therefore explain, in certain cases, the lower appar- ent prevalence in females of this age group.

It is a very common observation that males are more susceptible to parasitological infections than females

376

(BUNDY, 1988). In the case of filariasis, the question is slums in the city (ALBUQUERQUE, 1993). This means that whether females are more resistant to the infection or less control strategies must be adapted to existing urban con- exposed to infected vectors. A difference in exposure to ditions and directed to endemic communities as a whole, C.- quinquefasciatus could be explained only by dif- otherwise the endemic will probably expand in the city in ferences in behaviour and habits between the 2 sexes. in the next few years. the household and peri-household environment. ’

We observed in the communities studied that, quite frequently, males stay outside the houses after dinner talking and playing dominoes. There, close to open water drains and uncovered cesspits, transmission must cer- tainly occur intensely.

The prevalence of acute disease (1.9%2.0%) was slightly higher than that reported in other endemic areas (PANI et al., 1989), and may be considered a marker of the high level of transmission, an observation that may be useful for future evaluation of filariasis control pro- grammes.

The overall prevalence of filarial disease among the communities in Recife (6.3%) was relatively lower than one would expect, based on the microtilaraemia prevalence of lo%, since disease prevalence is typically higher than the point prevalence of microfilaraemia (BUNDY et al., 1991). This situation could have resulted from the long-term effect of individual treatment in pre- venting or greatly reducing clinical disease, even when it has not been possible to interrupt or reduce transmission. Control activities in Recife were started in 1954 and have basically consisted of treatment of mf carriers with DEC. Between 1982 and 1993. for examnle. 84 631 individuals were given DEC and 5 277 201 DEC tablets were used (MINISTERIO DA SA~DE, 1990, 1993). This could also explain the high frequency of subjects with mf densitv < 100 mfi60 uL found in this survey.

The prevalence of chronic manifestations was age- dependent in both sexes, reaching 11.3% in people aged 55-65 years. This pattern is similar to that found in Pon- dicherry, south India (PANI et al., 1989, 1991), and could be due to the accumulation of chronic cases in the population (SRIVIDYA et al., 1991). We also found that most lymphoedema and elephantiasis cases had lower limb in- volvement and hydrocele was the commonest chronic manifestation observed.

In our survey, 15.7% of the chronic disease patients were mf carriers. A recent study demonstrated by ultrasonography that lymphatic functional damage could de- velop in the lymphatics of asymptomatic microfilaraemic individuals (AMARAL et al., 1994), corroborating the hy- pothesis of the existence of 2 alternative routes leading to lymphatic pathology (OTTESEN, 1992), one dependent on a host immune response to the parasites leading to in- flammatory pathology without microfilaraemia and the other secondary to the presence of adult worms inducing local immunosuppressive responses. This last pathway would be expressed by individuals manifesting both lymphatic pathology and microfilaraemia (OTTESEN, 1992).

Nevertheless some authors explain the simultaneous chronic lymphatic pthology and microfilaraemia by re- infection of diseased persons. Consequently, the prob- ability of microfilaraemia associated with chronic disease is related to the local incidence of infection (BUNDY et al., 1991) and in some highly endemic areas one can often see patients with hydrocele and elephantiasis who are also microfilaraemic (WHO, 1992).

In Recife the prevalence of microfilaraemia among chronic patients could be the expression of a high level of transmission. We may conclude that the epidemiological pattern of filariasis in the population studied was characterized bv high nrevalence of microfilaraemia, low mf density in inf&ted people, and relatively low prevalence of filarial disease. Filariasis control campaigns have not been able to disrupt transmission. However, they could have had a long-term effect on the prevalence of clinical disease.

The maintenance of endemic tilariasis in Recife is cer- tainly associated with the low quality of life in most of the urban areas, manifested by the great number of

Acknowledgements We are grateful to Dr D. A. I’. Bundy for critical reading and

helpful comments and Mrs Luciana da Fonte for reviewing the references.

This investigation received financial support from the UNDPiWorld Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR), Conselho National de Pesauisa ICNPa). and FundacHo de Amoaro B Ciencia e Tec- nologia’de Pernamb%co (FACEPE):

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TRANSACTIONS OF nx ROYAL SOCIETY OF TROPICAL MEDICINE AND HKIENE (1995) 89, 377-378

Serological evidence for the presence of toxocariasis in the Turkana District of Kenya

J. V. Kenny’, R. J. MacCabe2, H. V. Smith3 and C. Holland4 ‘Department of International Health and Tropical Medicine, Royal College of Surgeons in Ireland, St Stephen’s Green, Dublin 2, Republic of Ireland; 2P.0. Box 1.5, Lokitaung, Turkana, Kenya; 3Scottish Parasite Diag- nostic Laboratory, Department of Bacteriology, Stobhill General Hospital, Glasgoy, G21 3UW, Scotland, UK; 4Department of Zoology, Trinity College, Dublin 2, Repub- lic of Ireland

Keywords: toxocariasis, Toxocara canis, Kenya

Toxocariasis is caused by infection with the ova of the dog round worm Toxocara canis. Clinical symptoms are usually non-specific except for ocular larva migrans (OLM), which can be misdiagnosed as retinoblastoma, a malignant tumour of the eyes. Serodiagnosis is, therefore, important for detecting possible cases of human toxocariasis. An enzyme-linked immunosorbent assay (ELISA) has been shown to be highly sensitive and specific for T. canis infection (DE SAVICNY et al., 1979). There are no published statistics on the prevalence or incidence of toxocariasis in Turkana, a district of north- west Kenya; however, rates of human infection with the larvae of the dog tapeworm Echinococcus granulosus of between 4.1% to 16.4% have been recorded in the north- east of Turkana District (KENNY & MACCABE, 1993). Although infective ova passed in dog faeces would be ex- pected to perish quickly in an arid environment such as Turkana, studies by WACHIRA et al. (1991) have shown that E. granulosus ova can survive for prolonged periods. The intimate association between dogs and Turkana nomads should also facilitate the survival of T. canis ova, despite their different life cycle. Furthermore, the capac- ity of T. canis for vertical transmission ensures that al- most all pups are infected at birth and therefore provide a high risk for human infection. Table. Prevalence of antibodies to Toxocara canis excretory- secretory antigens in sera of a population in Turkana, Kenya, according to age

O-9 lo-19 Age group (years)

20-29 30-39 40-49 250 Total

Negative 90 38 29 32 14 8 211 (92.5%) Positive 4 Total 94 402 3: 3: 1:

2 17 (7.5%) 10 228 (100%)

Materials and Methods The local Turkana chiefs were consulted and agreed to

co-operate in studies aimed at gathering prevalence data. During routine visits to nomadic watering holes by the Lokitaung mobile health unit, blood samples were collected from the nomads on filter paper and stored for analysis. The name, age, sex and location of each person were recorded directly on the filter paper. This technique has been shown to be effective and valid in field studies in remote areas (KENNY, 1993). Two hundred and twenty-eight dried filter blood spots were tested using the ELISA technique described by SMITH (1993) for the presence of antibodies to T. canis excretory-secretory antigens (TES). Briefly, two 3 mm spots were punched out of each dried blood spot and were placed in individual wells of micro-ELISA plates (Dynatechm M129) pre- viously coated with TES at optimal concentration (3 FgimL). Doubling dilutions of each sample (starting dilution 1:50) were placed in the wells (1:50 was chosen to minimize cross-reactivity with other blood products; SMITH et al., 1987). Each 3 mm disk contained an equi- valent of 2.5 PL of blood. Serum proteins were eluted in 125p.L of diluting buffer (150 mM phosphate-buffered saline, pH 7.2, containing 0.05% Tween 20@) by shaking on a horizontal shaker for 2 h; 50 PL aliquots of each sample were examined by ELISA.

Results Two hundred and eleven (92.5%) blood spots were

below the 1:50 cut-off titre; 17 (7.5%) were positive, with titres ranging from 1:50 to 1: 100 (Table). Six (35.3%) of the samples with antibodies to TES had also been shown to contain anti-Echinococcus antibodies in a previous study (KENNY & MACCABE, 1993).

Discussion This is the first record of the presence of antibodies to

TES amongst the Turkana nomads. Morbidity statistics from the Lokitaung mobile laboratory show eye com- plaints to be very common amongst the Turkana, and the extraordinary attachment of the nomads to their dogs should alert us to the possibility of human infection with T. canis ova. A recent study of 900 people in Turkana found 6.8% to be suffering from monocular blindness, suggesting that up to 14 000 people may be afflicted throughout the area (LOEWENTHAL & PE’ER, 1990). No reference was made to OLM, but the authors stressed that the absence of specialist ophthalmologists in the Turkana region creates particular difficulties in diagnosis and treatment of ophthalmic conditions. The possibility of misdiagnosis of toxocariasis exists even where facilities are good. For example, in a study of 500 consecutive patients referred by ophthalmologists to an oncology clinic in the USA for specialist eye examination, SHIELDS et al. (1991) found that 42% had lesions which simulated reti-

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