Seasonality, parity rates and transmission indices of Mansonella ozzardi (Manson) (Nematoda: Onchocercidae) by Cerqueirellum argentiscutum (Shelley & Luna Dias) (Diptera: Simulidae) in a lower Solimões River community, Amazonas, Brazil

Sazonalidade, taxa de paridade e índices de transmissão de Mansonella ozzardi (Manson) (Nematoda: Onchocercidae) por Cerqueirellum argentiscutum (Shelley & Luna Dias) (Diptera: Simuliidae) em uma comunidade do baixo rio Solimões, Amazonas, Brasil

CIÊNCIAS DA SAÚDE

Seasonality, parity rates and transmission indices of Mansonella ozzardi (Manson) (Nematoda: Onchocercidae) by Cerqueirellum argentiscutum (Shelley & Luna Dias) (Diptera: Simulidae) in a lower Solimões River community, Amazonas, Brazil¹

Sazonalidade, taxa de paridade e índices de transmissão de Mansonella ozzardi (Manson) (Nematoda: Onchocercidae) por Cerqueirellum argentiscutum (Shelley & Luna Dias) (Diptera: Simuliidae) em uma comunidade do baixo rio Solimões, Amazonas, Brasil

Jansen Fernandes de Medeiros; Victor Py-Daniel

Instituto Nacional de Pesquisas da Amazônia, Coordenação de Pesquisas em Ciências da Saúde, Laboratório de Filarioses e Vetores, C.P. 478, 69011-970, Manaus, AM, Brasil, E-mail: [e-mail], [e-mail]

ABSTRACT

Mansonella ozzardi is transmitted by two dipterian families, Ceratopogonidae (midges) and Simuliidae (black flies). In Brazil, black flies are vectors for this filariasis until now. In this paper, we determined the seasonality, parity capacity and parasitic infection rate of Cerqueirellum argentiscutum. The work was carried out in the Porto Japão community, Lower Solimões River, Amazonas, Brazil. Results show that the black flies were more abundant during the rainy season (from December to May). The number of parous flies was higher in every sampling during the course of year. Monthly Biting Rate (MBR₁ 123742.00, MBR₂ 86701.50) was high, although Parasitic Infection Rate (PIR₁ 0.06, PIR₂ 0.08) and Annual Transmission Potential (ATP 7.25) were low in numbers.

Key words: Simuliidae, Mansonella ozzardi, Amazônia, Brazil.

RESUMO

Mansonella ozzardi é transmitida por dois grupos distintos de insetos, Ceratopogonidae e Simuliidae. No Brasil, os simulídeos são os vetores dessa filariose. Neste trabalho, o objetivo foi determinar a sazonalidade, a paridade e a taxa de infecção parasitária de Cerqueirellum argentiscutum. O experimento foi realizado na comunidade Porto do Japão, Baixo rio Solimões, Amazonas, Brasil. Os simulídeos foram mais abundantes no período de chuva (dezembro a maio). Em todos os meses de coletas o número de paríparas foi maior. A taxa mensal de picada (TMP₁ 123742.00, TMP₂ 86701.50) foi elevada, já a taxa de infecção parasitária (TIP₁ 0.06, TIP₂ 0.08) e o potencial de transmissão anual (PTA 7.25) foram considerados baixos.

Palavras-chave: Simuliidae, Mansonella ozzardi, Amazônia, Brasil.

INTRODUCTION

Mansonella ozzardi is the filarial agent of mansonelliasis. The first report of this disease was made by Manson in 1897, in Guiana. According to Batista et al. (1960) and Oliveira (1961), people infected with mansonelliasis and high microfilaremia present symptoms of moderate fever, articular pain, adenite (followed by dizziness) and headaches. A new sintomatology attributed to this filariasis is the occurrence of visual lesions, which in turn can lead to blindness (Branco et al., 1998, Garrido & Campos, 2000).

This filariasis is found from Mexico to Argentina, Guatemala and Panama in Central America, and also some islands of the Antillean archipelago. Except for Chile, Uruguay and Paraguay, every country in South America has already reported the presence of this parasite (Tavares & Fraiha Neto, 1997).

M. ozzardi is transmitted by insects of the families Ceratopogonidae and Simuliidae, Diptera. Initial work accomplished by Buckley (1934) indicated Culicoides furens (Poey) (Ceratopogonidae) as the vector of M. ozzardi in St Vincent Island, Caribbean. C. furens was later revealed as a vector in Mexico and Trinidad (Biagi et al., 1958), whereas C. phlebotomus (Williston) was the vector in Haiti (Nathan, 1978, Lowrie & Raccurt, 1981).

In Colombia, Simulium sanguineum [= Cerqueirellum sanguineum (Knab)], S. amazonicum [= C. amazonicum (Goeldi)], S. argentiscutum [= C. argentiscutum (Shelley & Luna Dias)] and Culicoides insiniatus Ortiz & Leon have been reported as likely vectors of M. ozzardi (Tidwell et al., 1980, Tidwell & Tidwell, 1982). S. sanguineum [= C. sanguineum (Knab)], S. minusculum [= Psaroniocompsa incrustata (Lutz)] and S. sanchezi [= C. oyapockense (Floch & Abonnenc)] were indicated as vectors of M. ozzardi in south Panama, Guyana and Venezuela, respectively (Nathan et al., 1982, Peterson et al., 1984, Yarzábal et al., 1985). Shelley & Coscarón (2001) observed in S. exiguum [= Notolepria exiguua (Roubaud)] and Culicoides lahillei (Iches) the microfilarial development of M. ozzardi to the infective stage (L₃) in (northern) Argentina.

Early assessment by Cerqueira (1959) indicated S. amazonicum [= C. amazonicum] as a vector of M. ozzardi in Brazil. However, Moraes et al. (1985) suggested that the species identified in that work was probably S. argentiscutum [= C. argentiscutum]. Shelley & Shelley (1976) also reported S. amazonicum [= C. amazonicum] as a vector of M. ozzardi, while Shelley et al. (1980) indicated not only S. amazonicum [= C. amazonicum], but also S. argentiscutum [= C. argentiscutum] involvement in the transmission of mansonelliasis. Moraes et al. (1985) indicated S. oyapockense [= C. oyapockense] as a vector in the State of Roraima, Brazil.

In Brazil, the first report of M. ozzardi was made by Deane (1949). Lacerda & Rachou (1956) provided evidence that this filaria is found in the State of Amazonas, in the communities bordering the Solimões River and its tributaries.

The goal of this work is to assess the seasonality, the parity and the transmission indices of C. argentiscutum one of the vectors of M. ozzardi in Brazil. This is the first work considering the range of a 1-year sampling of C. argentiscutum. This work follows the nomenclature according to Py-Daniel & Moreira Sampaio (1994), where the subgenus is elevated to genus level in Simuliidae.

MATERIALS AND METHODS

Study area

This work was conducted from September 1999 to August 2000, in the Porto Japão community (3º 34" S / 61º 09" W), lower Solimões River, Amazonas, Brazil. The community has approximately 100 people, subsisting on fishing, hunting and farming.

Procedure of Capture

The black flies were collected monthly during four consecutive days starting at 6:00 and ending at 18:15. The sampling intervals were divided into 15-minute periods, each followed by 15-minute intervals. They were captured by a laboratory technician, using manual suction collectors, according to the methodology of Medeiros & Py-Daniel (1999) and Medeiros & Py-Daniel (2003).

Analysis of the Ovaries

Between samplings, we analysed the ovaries to verify whether the females were nulliparous or parous, according to the methodology of Ramirez-Perez (1977). The flies were then placed in tubes containing 70% ethanol, for later examination at the Laboratório de Filarioses e Vetores of the Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil.

Dissection of the black flies

The flies were immersed in acid hematoxilin and stained for a period of 48 hours, prior to dissection under a stereomicroscope. They were placed on a slide, divided in three parts (head, thorax and abdomen), placed in a drop of a glycerin and covered by a coveslip. The slides were then observed by light microscopy, and the flies were verified for mansonelliasis infections. When the parasites were found, the developmental stages (mf, L1, L2, L3) were identified according to the method of Yarzábal et al. (1985).

Parasitic Infection Rate (PIR)

Two methods were used to obtain this index: PIR₁, considered the number of females infected by any filarial stage (mf, L1, L2 and L3) of M. ozzardi divided by the number of parous females and dissected nulliparous X 100; PIR₂ considered the number of females infected with any filarial stages, except microfilaria (L1, L2 and L3) of M. ozzardi divided by the number of parous females dissected X 100 (Py-Daniel et al., 2000).

Monthly Biting Rate (MBR)

This index estimates the number of black flies that bite a person exposed in the same place for a month, subjected to bites all day long (Davies & Crosskey, 1991). Two ways of calculating MBR were taken into account: one considers the total of captured females (nulliparous + parous) while the other considers only the parous females (Py-Daniel et al., 2000).

Monthly Transmission Potential (MTP)

This index estimates the number of L3 stage larvae that can be transmitted to a person exposed to the vector during a one month period (Duke, 1968, Davies & Crosskey, 1991).

Annual Transmission Potential (ATP)

represents the number of L3 stage larvae that can be transmitted to a person exposed to the vector during a one year period (Davies & Crosskey, 1991). It is calculated by the sum of all MTPs (Monthly Potential Transmission) (Py-Daniel et al., 2000).

Prevalence

Approximately 80% of the habitants in Porto Japão were examined. A lancet was used to puncture the fourth finger of individuals and a drop of blood was used to make a thick film on a microscope slide. The film was de-ha emoglobinized, fixed in 80% methanol, and later stained with Giemsa and examined for microfilariae.

Additional Information

Ribeiro & Adis (1984) consider two seasons for the Central Amazon, a dry season between June and November and a rainy season from December to May.

The statistical analyses were performed as non-parametric tests, using the Mann-Whitney (U-test).

RESULTS

Seasonality

16320 C. argentiscutum females were collected throughout this work, with an average of 1360 individuals per month and 340 individuals per day. The highest number of simuliid flies was obtained during the rainy season (from December to May), with 13488 (82.65% of the total collected flies) (2248 ± 1373.9 flies/month / 562 ± 366.3 flies/day), showing a statiscally significant difference (U = 325 P < 0.001) in relation to the number of flies collected in the dry season (from June to November) with a total of 2832 individuals (472 ± 305.4 flies/month / 118 ± 86.3 flies/day), approximately 17.35% of the total (Table 1).

During the rainy season, the highest incidence of simuliid flies was reported from December 1999 to February 2000, resulting in a total of 9753 specimens (59.76% of the total/year), (3251 ± 1290.2 flies/month / 813 ± 363 flies/day). In the dry season, the highest number of black flies was obtained in September/1999, November 1999 and June 2000, resulting in a total of 1994 individuals (8.53% of the total/year) (664.6 ± 306 flies/month / 166.1 ± 94 flies/day).

The highest number of individuals was collected in January (1021.5 ± 239.3 flies/day), corresponding to approximately 25% of the total. The lowest number of individuals was sampled in July (23 ± 18.3 flies/day), corresponding to approximately 0.56% of the total flies collected throughout this study.

Ovarian physiological stage

A total of 11441 parous females (70.1%) and 4879 nulliparous females (29.9%) were collected. The abundance of parous flies over the nulliparous flies was verified in every month of the year (Figure 1).

Parasitic Infection Rate - PIR

Only nine out of the 16.320 collected flies were infected by M. ozzardi, representing a Parasitic Infection Rate (PIR₁) of 0.06%, and a PIR₂ of 0.08%. The highest number of infected simuliid flies was found in January and February. The highest PIRs was reported in July (Table 2).

A total of 34 M. ozzardi larval stage was found in the black flies collected, with a higher number of L2 stage (17), followed by L1 (16) and L3 (1). All the larval stages of M. ozzardi were found in the thorax of the flies.

Monthly Biting Rates MBR, Monthly Transmition Potential - MTP and Annual Transmission Potential - ATP

The estimated Monthly Biting Rate (BMR₁) was 124.521,25 bites/person-month and BMR₂ was 87.348,75. Both BMR₁ and BMR₂ were higher in January (31.674,25) and February (30.232,75) while lower BMRs were reported in July (690,0) and August (2.549,75) (Table 2).

The MTP was only calculated for February, when a L3 stage was found in an infected black fly. Therefore, the calculated MTP has the same value as the ATP, i. e., 7.25 (Table 2).

DISCUSSION

The lowest number of flies collected in July was due to a cold mass movement in the first two days of sampling, when strong winds (up to 22,4 Km/h) were verified in the area, followed by low temperatures and high relative air humidity.

Our results agree with statements of the local population where the work was carried out, corroborating the fact that the highest number of black flies occur in months of higher precipitation. Cerqueira (1959) in a work developed in the city of Codajás (Middle Solimões River), Amazonas, the largest density of S. amazonicum [= C. argentiscutum] was also found during the rainy season, considered by him to be from January to June.

Medeiros & Py-Daniel (1999) verified a higher abundance of the species C. oyapockense, in Xitei/Xidea, in the Yanomami indigenous area, Roraima, Brazil, in the period of higher precipitation. Shelley (1988) working in Toototobi and Shelley et al. (1997), in Catrimani (both Yanomami areas) reported that the highest number of S. oyapockense [= C. oyapockense] was observed during the rainy period.

The present results provided evidence that C. argentiscutum was more abundant in the beginning of the rainy season (from December to February), subsequently decreasing in numbers from March to May, and at the beginning of the dry period (June and July) when the Solimões River is flooded. We observed that from May to July, when the floods reached the forest, the populations of C. argentiscutum migrated to the inundated area (also called várzea), where a higher prevalence of the simuliids were found, correlated with a decrease in the number of specimens sampled alongside the river. It may be suggested that females of this species migrate to the várzea area as a survival strategy, to have access to other sources of blood.

The high number of parous flies collected in this work is probably related to the anthropophilic behavior of C. argentiscutum and their high chances of finding a host (man), taking into account the working habits of the local people (setting up agricultural crops at the margins of the river, being exposed daily to the biting activity of this species). Medeiros & Py-Daniel (1999) found 84% of parous female of C. oyapockense in Xitei/Xidea; and Shelley et al. (1997), collected a higher number of S. oyapockense [= C. oyapockense] parous females (79.3%) as compared to the nulliparous females (20.7%) in Toototobi.

In a previous report involving several streams in the city of Codajás, Cerqueira (1959) indicated for S. amazonicum [= C. argentiscutum] a distinctive parasitic infection rate for the various places, totaling 18.5% of the 1367 individuals captured. Shelley & Shelley (1976) found a natural infection rate for S. amazonicum [= C. amazonicum] estimated in 0.99%, representing 35 individuals out of 3530 collected in humans and bovine cattle, while working in two villages located on the Purus River, close to the municipality of Lábrea, Amazonas. Shelley et al. (1980) found S. amazonicum [= C. amazonicum] and Simulium n.sp [= C. argentiscutum] naturally infected with M. ozzardi, with a parasitic infection rate of 3.1% and 9.7%, respectively (Ticuna tribe, Solimões River, Amazonas).

By comparing the Parasitic Infection Rates (PIR) of the published works cited above, we can say that the PIR values observed in this work are low, particularly in relation to the findings of Cerqueira (1959) and Shelley et al. (1980). The low rates (PIR₁ and PIR₂) found in this work are probably due to the of absence of mansonelliasis in the community of Porto Japão (0% prevalence, in 80% of the examined population). The black flies found infected are most likely to be related to factors such as periodic visits (migrations) of people infected with mansonelliasis from other communities located in the Middle and Upper Solimões River, considering the fact that daily movement of ships takes place on the river.

In Brazil, reports on the M. ozzardi vectors have not been considering systematic collection (Cerqueira, 1959, Shelley & Shelley, 1976, Shelley et al., 1980, Moraes et al., 1985), and therefore, for comparisons of the Monthly Biting Rate (MBR), we considered some works on species involved in the transmission of the filarial worm Onchocerca volvulus (Leuckart) in the indigenous Yanomami area, Roraima, Brazil (Andreazze & Py-Daniel, 1999, Py-Daniel et al., 2000).

Andreazze & Py-Daniel (1999) in the Xitei/Xidea area, determined a MBR₁ of 63.079,7 and a MBR₂ of 37.394,5 for the species P. incrustata. Py-Daniel et al. (2000) found a MBR₁ of 28.443,0 and a MBR₂ of 18.360,2 in a work conducted in the same place with the species T. guianense. Py-Daniel et al. (2000) also estimated the MBR for the four species (P. incrustata, T. guianense, C. oyapockense and N. exiguua) occurring in Xitei/Xidea, and found a MBR₁ of 92.931,7 and a MBR₂ of 56.936,5.

By comparing the MBRs between these two areas (Porto Japão and Xitei/Xidea), we observed that in Porto Japão, MBRs in only one species was higher than the total MBRs calculated for the four species of Xitei/Xidea area. Therefore, the species C. argentiscutum, in some periods of the year, such as January and February, represents a plague for the population living alongside the Solimões River due to the high density of flies and consequently, the discomfort of their bites.

The fact that only one metacyclic larva (L3 stage) was found in February indicates a low ATP for this area, suggesting that a low transmission risk of M. ozzardi exists for the population of the study area. According to an index established by the World Health Organization for the vectors of O. volvulus, the estimated level in order to maintain transmission is around 100 L3 larvae per person during one year (Davis et al., 1994), which is not yet known for M. ozzardi vectors.

ACKNOWLEDGEMENTS

We thank INPA for support, CNPq for the PhD scholarship for the first author, and the Porto Japão community, especially Mr. Aníbal César B. Lima for excellent assistance in the black fly samplings and dissections.

LITERATURE CITED

Recebido em 23/01/2004

Aceito em 19/04/2004

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1

This work is part of the first author's PhD Thesis

Publication Dates

• Publication in this collection
  22 Sept 2004
• Date of issue
  2004

History

• Accepted
  19 Apr 2004
• Received
  23 Jan 2004