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Commercial coconut palm as an ecotope of Chagas disease vectors in north-eastern Venezuela.

Introduction

Trypanosoma cruzi (Kinetoplastida: Trypanosomatidae), the causal agent of Chagas disease, develops in an ecopathogenic complex in which the parasites circulate between numerous selvatic mammalian reservoirs and insect vectors (Hemiptera, Reduviidae, Triatominae). Both bioecological and social factors promote the dispersion of this wild enzootia, facilitating the development of the so called peri- and domestic transmission cycles in which humans and several domestic mammals act as reservoirs of the disease. In addition, a few triatomine species have become adapted to colonize houses, including those in highly urbanized areas (1-2). Despite the importance of T. cruzi for public health, basic aspects of its sylvatic and peridomiciliar transmission cycle have not yet been fully elucidated (3).

Among the numerous triatomine ecotopes, palms (Palmae) are possibly the most extensively studied. Nevertheless, although the infestation of many palm species has been widely reported for Venezuela, there are few reports of Coccus nucifera (coconut palm) as an appropriate vegetal niche for triatomines (4-10). Rhodnius pallescens has, however, been found colonizing coconut palms in Colombia (3,11). These reports led us to investigate the role of commercial coconut palms as niches for triatomines in peridomiciliar ecotopes in endemic rural areas of north-eastern Venezuela.

Material & Methods

Study areas: The study was carried out in the following villages: Eneal I, Eneal II, Valle del Neveri, Pica del Neven, Guaipalomo and Angostura (Bolivar Municipality; north Anzoategui State, Venezuela). All the villages surveyed (10[degrees] 08' N--64[degrees] 37' W) lie just six meters above sea level, in a dry littoral tropical forest biome with humidity coming from the mountains. The temperature ranges from 25-29[degrees]C, mean annual rainfall 500-600 [mm.sup.3] and 75-85% relative humidity (12). There were a total of 112 houses and 320 people in the study area. Coconut palms were randomly selected in a radius of 1-5 m from inhabited houses with improved construction. Sampling was done from January 2008 to July 2009.

Dissection of palms and isolation of Trypanosoma spp from collected triatomines: A total of 14 C. nucifera palms ([bar.x] =19 yr old) were studied (4). Dry and green leaves, humid debris, interfoliaceus meshes and bracts were examined for the presence of triatomines. Collected adult triatomines and first and fifth instars were identified according to Lent and Wygodzinsky (13). Other stages were identified in the laboratory by the ontogenical sequencing of collected specimens.

Insectivorous bats (Eumops glaucinus, Molossidae; Glossophaga longirostris, PhyllostomidaeGlossophaginae), and opossums (Didelphis marsupialis) were found in several palms.

Samples of the intestinal content of triatomines macerated in isotonic saline solution and triatomine haemolymph were examined microscopically as wet smears (400x) and Giemsa-stained smears (1000x) for the presence of Trypanosoma (7,14). Fecal material from positive triatomines was inoculated subcutaneously (200 metacyclic trypomastigotes/g body weight) into groups of five NMRI mice raised at our laboratory facilities ([bar.x] = 12 g wt). Tail blood samples were examined three days after inoculation and thereafter three times weekly until the onset of chronicity or death (15,16).

The identification of Trypanosoma species was performed by xenodiagnosis of positive mice with 12 reared III instar nymphs of R. prolixus in order to observe the typical T. cruzi and/or T. rangeli triatomine-mammal-triatomine cycle (7,14). Blood parasites were cultured first in blood agar medium (Difco, Thomas Scientific, New Jersey, USA) in a 5-fluorocytocin and gentamycin solution and then in Roswell Park Memorial Institute Medium (RPMI) at 27[degrees]C. Haemolymph flagellates from naturally infected triatomines were maintained using the same protocol.

Molecular characterization of Trypanosoma isolates: DNA extraction and polymerase chain reaction (PCR) for amplification of the D7 divergent domain of the 24S[alpha] rRNA gene (D71, 5'-AAGGTGCGTCGACAGTGTGG-3' and D72 5'TTTTCAGAATGGCCGAACAGT-3' primers); the non-transcribed spacer of the mini-exon genes (TC 5'-CCCCCCTCCCAGGCCACACTG-3', TC1 5'-GTGTCCGCCACCTCCTTCGGGCC-3' and TC2 5'CCTGCAGGCACACGTGTGTGTG-3' primers) and the size-variable domain of the 18S rRNA gene (V1, 5'-CAAGCGGCTGGGTGGTTATTCCA-3' and V2, 5'-TTGAGGGAAGGCATGACACATGT-3' primers), were performed following the Brisse et al protocols (17) for the following codified triatomine isolates (18): TPRX/VE/2008/ANG; TPRX/VE/2009/ ANG78; TPRX/VE/2009/El1; TPRX/VE/2009/El3; TPRX/VE/2009/El12; TMAC/VE/2008/Piq1; TMAC/VE/2008/Pique62; and TMAC/VE/2008/ Pique63.

Identification of the blood meal sources of collected triatomines: Blood meal sources were determined for 105 T. maculata and 101 R. prolixus randomly selected from those collected in the coconut palms, using an enzyme-linked immunosorbent assay (ELISA). Briefly, the intestinal contents of the triatomines were incubated for 1 h at 18[degrees]C and then left to dry on paper. Then, 5 of 5% bovine serum albumin (BSA) were added and the mixture was incubated for a further 1 h at 18[degrees]C. The paper disks were inserted in an ELISA plate with 150 [micro]l of commercial anti-rabbit IgG, anti-mouse IgG, anti-rat IgG, anti-hen IgG, anti-horse IgG, anti-human IgG and anti-dog IgG conjugated to alkaline phosphatase (Santa Cruz Biotechnology, Inc. Antibodies), or with artisanal antisera from opossum blood sera produced in New Zealand albino rabbits and conjugated to alkaline phosphatase; all paper disks were washed after incubation.

The conjugated antisera were diluted (1/1000) in PBS pH 7.2-Tween20, 0. 05-5% low fat milk and incubated for 30 min at 37[degrees]C, 150 [micro]l of p-nitrophenyl phosphate in diethanolamine buffer (DEA) were then added and the mixture incubated for a further 20 min. The reaction was stopped with 1M NaOH (100 [micro]l/ well) and read at 405 nm in an ELISA Spectra Classic (TECAN, Austria). The cut-off value for a positive reaction with commercial conjugates was OD (optical density) = 0.2 and with opossum conjugates, OD = 0.4. The intestinal content of reared R prolixus fed on blood from different animals, was used as a control.

Ethical guidelines: The experiments involving animals in this study comply with the current laws of Bioethics as set down by the Venezuelan Ministry of Science and Technology, and were approved by the Ethics Review Committee and Animal Management Committee, FONACIT (Fondo Nacional para la Ciencia y Tecnologia).

Statistical analysis: The data were processed using the Microsoft Excel program and analyzed with either ANOVA, the Kolmogorov-Smirnov test or simple regression, according to each particular case. All tests were done using the Statgraphics 5 Plus software.

Results

Palms from six villages in north-eastern Venezuela (n=14, mean height = 18.2 m) were identified as Coccus nucifera Linneo (Palmae) or 'coconut palm', native to tropical ecosystems in both the Old and New Worlds (19). The palms had a mean of 35 dry leaves, 30 green leaves and 12 bracts.

Hatched and fresh triatomine eggs (0-245; mean = 53 eggs/palm) were observed in all the plant parts examined, except for the green leaves, of 13/14 palms. Of the physiognomic characters tested, the only correlation found was a strong positive correlation between palm length and the number of triatomine eggs (simple regression, r = 0.704465, Table 1).

Overall, 242 R. prolixus and 144 T. maculata adults were found in 11 out of the 14 palms examined. There were no significant differences in the distribution of instars (relative abundance of individuals in each instar) among palms for either of the triatomine species studied (F = 0.72861, p > 0.05, df = 5, for R. prolixus; and F = 0.409013, p >0.05, df = 5 for T. maculata) (Table 2). A strong positive correlation (r = 0.704465) between palm height (11.8-32 m) and the number of individuals successfully raised from viable eggs to adult (in the laboratory) was found.

Almost all of the R. prolixus individuals collected were infected by T. cruzi (98%), while the proportion of infected T. maculata individuals was lower (70%) (Table 2). In addition, 13% of R prolixus were infected by both T. rangeli and T. cruzi according to parasitological and/or molecular criteria (7,14,17) (Table 3). Trypanosoma rangeli was not, however, observed in T. maculata. Our attempts to maintain T. rangeli in RPMI medium were fruitless.

The number of individuals of each triatomine species in relation to their alimentary sources is shown in Fig. 1. According to the ELISA analyses of the blood sources of T. maculata and R. prolixus, these species were eclectic in their alimentary habits; feeding on birds, rodents, opossums, rabbits, dogs and horses. Only R. prolixus rarely used humans as a blood source. There was no statistically significant difference between the frequency distribution of blood sources between the triatomine species (Kolmogorov-Smirnov test, p >0.05).

[FIGURE 1 OMITTED]

The results of the molecular analysis by PCR using the three molecular markers analyzed in T. cruzi isolates: the non-transcribed spacer of the mini-exon genes, the D7 divergent domain of the 24S[alpha] rRNA gene, and the size-variable domain of the 18S rRNA gene, showed an TcI lineage pattern as revealed by the amplification of the products at of 350, 110 and 175 bp, respectively, in the eight parasite strains isolated from collected triatomines (Figs. 2A, B, C).

Discussion

The natural foci of American trypanosomiasis are extremely diverse and notably ubiquitous due to the enormous variation in habitats and reservoirs of T. cruzi and the marked eurytopy and eurytrophy of the vectors (7).

[FIGURE 2 OMITTED]

The wide neotropical distribution of the palms, their varied antropic uses and morphological variability permits the formation of trophic chains; from invertebrates to poikilothermic and homeothermic vertebrates, which provide the triatomines with readily available reservoirs as blood sources. This explains why the palm-triatomine adaptation is the most suitable for the tribe Rhodniini, and thus the importance of the palms as natural ecotopes for this zoonosis (4,8,20,21). All these factors combined confer great ecoepidemiological importance to palms as environmental bioindicators of wild and peridomestic triatomine ecotopes and, consequently, as risk components for Chagas disease (3).

Reports of the presence of triatomines in commercial coconut palms, and more specifically the sympatric presence of R. prolixus and T. maculata in these palms in Venezuela, are scarce4. In this study, in spite of the low number of plants examined and insects collected, the infection percentages for T. cruzi in R prolixus and T. maculata (98 and 70%, respectively) can be considered high when compared with other results. In addition, the presence of T. rangeli in 13% of the collected R. prolixus demonstrates the importance of C. nucifera as an environmental bioindicator of areas with a high risk of transmission of both trypanosomes. The positive correlation between coconut palm height and viable triatomine eggs found in this study, suggests that both palm microclimate (temperature, ventilation and humidity) and vertebrate colonization are important for vector biogeocenosis.

Despite their high genetic variability, T. cruzi isolates have been classified into two major phylogenetic lineages, T. cruzi I and T. cruzi II based on zymodemes and different genetic markers (18,22-24). A preferential association of T. cruzi genotypes with sylvatic or domestic transmission cycles has been described. Parasites belonging to the T. cruzi II genotype are preferentially associated with human infection and domestic cycles in regions from the American Southern Cone where Chagas' disease is endemic (24-27), while T. cruzi I parasites are associated with the sylvatic cycle and a low prevalence of symptomatic patients (24,25,28). However, a recently published paper showed that 74% of Venezuelan isolates from acute chagasic patients were typed as T. cruzi I (29). Other studies also suggest that T. cruzi I predominates in both human and sylvatic cycles, at least in Mexico and Guatemala (30).

Trypanosoma cruzi II, was later subdivided into five groups: Tc IIa-IIe (18,30-32). Brisse et al (17) reported simple methods for the characterization of T. cruzi isolates by agarose gel electrophoreses of the PCR products with only three genes: mini-exon, 24S[alpha] rRNA, and 18S rRNA. This approach was used in this investigation and we obtained only the TcI pattern. A Second Satellite Meeting in 2009 (33), recognized that the nomenclature for T. cruzi strains should be classified into six DTUs: T. cruzi I-VI. Trypanosoma cruzi I corresponds to the TcI originally defined in the First Satellite Meeting (18). The fact that only the TcI lineage was identified in this study (the most abundant lineage among chagasic patients in Venezuela), reinforces the hypothesis that both domestic and peridomestic transmission cycles may be sustained by triatomines from surrounding palms (29,34).

Nevertheless, the scarce participation of humans as food sources for either species (as revealed by the ELISA test) indicates that this vegetal niche, although near to human dwellings, remains a closed ecotope for domestic parasite circulation in the study area. Birds were very important blood sources for both triatomine species, which is to be expected since poultry breeding in domestic and peridomestic environments and the colonization of birds inside palms (natural ecotopes of Passeriformes) is a common feature of rural communities in this country.

Rodents, dogs and horses also provided significant blood meal sources. These mammals are locally predominant due to the anthropization of the environment and the domestication and maintenance of livestock near coconut palms. Some mammals, such as bats and rodents were found inside coconut palms, and thus may be considered as potentially important T. cruzi reservoirs (7). Nevertheless, the absence of some mammals as blood meal sources may be justified in function of their biomass, defensive behavior against triatomines, or that some antisera were not used. These results suggest that assessments of potential blood sources should be done in function of local epidemiological situations rather than a priori assumptions.

Rhodnius prolixus, T. maculata and P. geniculatus are the main vectors of T. cruzi in Venezuela. Although all these species are distributed throughout the country, they show successively lower grades of domiciliation. Rhodnius prolixus is the most proliferative and aggressive in its feeding habits and quick defecation and is responsible for the high incidence and dispersion of Chagas disease in Venezuela (5). The adult stages of both R. prolixus and T. maculata habitually migrate to human dwellings: 29% of the R. prolixus and 25% of the T. maculata individuals collected were taken near human houses. It is suggested that this result, together with the high rates of triatomine infection, could be a risk factor to be considered in addition to the properties of C. nucifera as an appropriate natural ecotope.

The coconut palm is distributed in Venezuelan forests and coastal areas. There are scarce reports of T. maculata in this palm species in these areas (4,6,34). Thus it is imperative that more research be undertaken into coastal C. nucifera as an ecotope for different triatomine species. The oral transmission of T. cruzi has produced Chagas disease outbreaks in Brazil and recently in Venezuela due to the consumption of sugarcane juice, fruit wine from the 'bacaba' palm (Oenocarpus bacaba), or other foods where triatomines are crushed in artisan factories together with the vegetable matter, contaminating it with metatrypo-mastigotes (35-37). To obtain 'coconut water' from C. nucifera, consumers habitually ingest the liquid by drinking directly from the perforated fruit, thus touching their mouths to it. Fruit clusters can remain stored during long periods before their consumption, thus increasing the possibility of triatomine fecal contamination. Furthermore, Marques (38) developed a culture medium using 'coconut water' in which T. cruzi proliferates with metatrypomastigote production; thus the possibility of oral T. cruzi transmission by drinking from the coconut in this manner should not be overlooked.

Conclusion

This study represents an important contribution to the scarce knowledge on commercial coconut palms (C. nucifera) as natural and appropriate vegetal niches for the breeding and multiplication of R. prolixus and T. maculata in Venezuela. Both of these species are important Chagas disease vectors, with high rates of T. cruzi (TcI) infection. We hope that the results obtained lead to improved surveillance and control, especially of the re-infestation of human dwellings from surrounding palms. The area studied has its own epidemiological and micro-environmental peculiarities resulting from the particular human activities and social patterns found in this region, factors which should be taken into account when control programs are being planned.

Acknowledgement

The authors would like to thank M.Sc. Nilsa Gonzalez for her assistance in laboratory and field work; Dr Ricardo Guerrero for the identification of the bats, Dr Marian Ulrich (in memoriam) and T.C.S Adrian Chang and Sergio Ribera for their help in the preparation of this manuscript. This investigation was supported by the Universidad Central de Venezuela (Grant CDCH No. PG-0331-4729-2006, Caracas, Venezuela) and the Fondo Nacional de Ciencia y Tecnologfa-FONACIT (Grant No. G-2005000, Caracas, Venezuela).

References

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Corresponding author:

Leidi Herrera, Laboratorio de Biologia de Vectores y Parasitos, Instituto de Zoologia y Ecologia Tropical, Facultad de Ciencias, Universidad Central de Venezuela. P.O. Box 47058, Los Chaguaramos, Caracas, Venezuela. E-mail: herrerleidi@yahoo.com

Received: 2 February 2010

Accepted in revised form: 2 April 2010

A. Morocoima (a), J. Chique (a), R. Zavala-Jaspe (b), Z. Diaz-Bello (b), E. Ferrer (c), S. Urdaneta-Morales (d) & L. Herrera (d)

(a) Centro de Medicina Tropical, Facultad de Medicina, Universidad de Oriente, Estado Anzodtegui, Venezuela; (b) Seccion de Immunologia, Instituto de Medicina Tropical Felix Pifano, Facultad de Medicina, Universidad Central de Venezuela, Caracas, Venezuela; (c) Instituto de Investigaciones Biomedicas y Departamento de Parasitologia, Facultad de Ciencias de la Salud, Universidad de Carabobo Sede Aragua, Maracay, Venezuela; (d) Laboratorio de Biologia de Vectores y Pardsitos, Instituto de Zoologia y Ecologia Tropical, Facultad de Ciencias, Universidad Central de Venezuela, Caracas, Venezuela
Table 1. Physiognomical characteristics and triatomine egg
infestation in coconut palms (Coccus nucifera) from villages in
north-eastern Venezuela

Villages           Dissected   Length   Approx.    No. of dry
                   palm No.     (m)     age (yr)     leaves

Eneal I                1        19.5       25          46
                       2        11.8       13          12
                       3        22         23          33
                       4        15         16          18
Eneal II               5        17.8       18          28
                       6        12.6       12          40
Valle del Neveri       7        15.7       14          43
                       8        18         23          30
Guaipalomo             9        20         20          47
                      10        14         13          30
                      11        21.5       22          25
Pica del Neveri       12        16.3       14          36
                      13        19         24          45
Angostura             14        32         26          56

Av.                             18.2       18.8        35

Villages           No. of green   No. of   No. of hatched
                      leaves      bracts   and fresh egg

Eneal I                  0          12          60
                        52          15         103
                        38          18          30
                        42          10           0
Eneal II                32          12          25
                        26           7          10
Valle del Neveri        36          11          14
                        43          16          80
Guaipalomo              21          17          10
                        46          11          15
                        32          18          72
Pica del Neveri         28          10          41
                        0            5          35
Angostura               23          12         245

Av.                     30          12          53

Table 2. Distribution of R. prolixus and T. maculata instars and the
relative proportion of individuals infected with T. cruzi/palm in
coconut palms from villages in north-eastern Venezuela

Palm         Rhodnius prolixus instars         Infected by
No.                                             T. cruzi

        I    II   III   IV    V    A   Total     No. (%)

1        2    1    4     4    0    2     13      11 (84.6)
2        0    1    3     4    2    3     13      13 (100)
3        2    2    5     5    1    5     20      20 (100)
4        0    0    0     0    0    0      0       0 (0)
5        1    2    3     4    1    3     14      13 (92.9)
6        0    0    3     2    0    0      5       5 (100)
7        0    1    2     3    1    4     11      10 (90.9)
8        0    1    6     3    0    3     13      13 (100)
9        1    0    3     3    0    4     11      10 (90.9)
10       0    0    0     0    0    0      0       0 (0)
11       6    4    7     8    6    5     36      36 (100)
12       7    9    7     5    5   10     43      43 (100)
13       0    0    0     0    0    0      0       0 (0)
14       8   10    6     5    3   31     63      63 (100)
Total   27   31   49    46   19   70    242     237 (98)

Palm         Triatoma maculata instars          Infected
No.                                            by T. cruzi

         I   II   III   IV    V    A   Total     No. (%)

1        1    1    1     2    1    2      8       5 (62.5)
2        0    0    1     3    3    3     10       7 (70)
3        1    0    1     1    0    1      4       2 (50)
4        0    0    0     0    0    0      0       0 (0)
5        1    0    0     4    1    2      8       5 (62.5)
6        2    1    0     3    3    3     12       3 (25)
7        1    1    1     3    4    2     12       5 (41.7)
8        0    1    2     3    2    1      9       4 (44.4)
9        0    0    1     2    3    1      7       4 (57.1)
10       0    0    0     0    0    0      0       0 (0)
11       0    0    0     0    0    0      0       0 (0)
12       4    6    4     4    5    8     31      28 (90.3)
13       5    7    4     3    4    6     29      24 (82.8)
14       1    3    2     1    0    7     14      14 (100)
Total   16   20   17    29   26   36    144     101 (70)

I-V --Larval instars; A--Adults.

Table 3. Distribution of R prolixus and the relative proportion of
individuals coinfected with T. rangeli/ palm from villages in
north-eastern Venezuela

Palm No.   I Instar   II Instar   III Instar   IV Instar   V Instar

1             0           0           1            2          0
2             0           0           1            1          0
3             0           0           1            0          0
4             0           0           0            0          0
5             0           0           1            2          0
6             0           0           0            0          0
7             0           0           1            1          0
8             0           0           1            1          0
9             0           0           1            1          0
10            0           0           0            0          0
11            0           0           0            0          0
12            0           0           0            0          0
13            0           0           0            0          0
14            1           2           1            0          1

Total         1           2           8            8          1

Palm No.   Adult   Coinfected by
                    T. rangeli

                   No.      %

1            0     3/13     23.1
2            1     3/13     23.1
3            1     2/20     10
4            0     0/0      0
5            0     3/14     21.4
6            1     1/5      20
7            1     3/11     27
8            1     3/13     23.1
9            0     2/11     18.2
10           0     0/0      0
11           0     0/36     0
12           0     0/43     0
13           0     0/0      0
14           7     12/63    19

Total       12     32/242   13.0
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Author:Morocoima, A.; Chique, J.; Zavala-Jaspe, R.; Diaz-Bello, Z.; Ferrer, E.; Urdaneta-Morales, S.; Herre
Publication:Journal of Vector Borne Diseases
Article Type:Report
Geographic Code:3VENE
Date:Jun 1, 2010
Words:4756
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