dipetalonema perstans

Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2000072071
ENVIRONMENTAL FACTORS A N D THE DISTRIBUTION OF MANSONELLIASES
I N SOUTHERN VENEZUELA
G Ó M E Z J . * & G U E R R E R O R.**
Summary:
Résumé : FACTEURS ENVIRONNEMENTAUX ET DISTRIBUTION DES
The distribution of mansonelliases and their relation to various
quantitative criteria were determined through the study of
1,057 subjects in 17 localities in ten regions of Amazonas State
and Bolivar State. The total prevalence among the blood samples,
determined through the Knott technique, was 1 8.54 %. 1 1.26 %
were parasited by Mansonella perstans, 9.93 % by Mansonella
ozzardi, and 2.63 % by both species. The average of
microfilaremia was 48.19 mf/mL of blood in /VI. perstans and
13.79 mf/mL in M. ozzardi. In the regions studied, A/I. ozzardi
has a wider area of distribution than M. perstans. Prevalence,
average number of parasites per host, and the infection index
have a positive and statistically significant correlation with the total
annual precipitation mean for each region for M. perstans; in the
case of M. ozzardi the quantitative parameters are positively
correlated with the altitude of each region, this correlation being
statistically significant. With respect to type of vegetation,
M. perstans had a higher infection index in Amazonian caatinga
transition in pluvial lowland forest, and M. ozzardi in
semideciduous forest of the alisio type. Therefore two types of
transmission, M. ozzardi-Simulium and M. perstans-Culicoides are
suggested.
MANSONELLOSES DANS LE SUD DU VENEZUELA
La distribution des mansonelloses et leurs relations à divers critères
quantitatifs ont été déterminés à partir de l'étude de I 057 sujets
dans 17 localités de dix régions des États d'Amazonas et de
Bolivar, la prévalence dans les prélèvements sanguins, déterminée
selon la technique de Knott, était de 18,54 %. 11,26 % étaient
parasités par Mansonella perstans, 9,93 % par Mansonella
ozzardi, et 2,63 % par les deux espèces, le taux moyen de
microfilarémie était de 48, 19 mf/mL pour M. perstans et de
13,79 mf/mL pour M. ozzardi. Dans les régions étudiées,
M. ozzardi a une aire de répartition plus vaste que M. perstans.
Pour M. perstans, la prévalence, le nombre moyen de parasites et
l'index d'infection ont une corrélation positive et statistiquement
significative avec la moyenne des précipitations annuelles de
chaque région. Dans le cas de M. ozzardi, les paramètres
quantitatifs sont carrelés de façon positive et statistiquement
significative avec l'altitude de chaque région. Au regard du type
de végétation, l'index d'infection de M. perstans est plus élevé
dans lest forêts basses et humides, et celui de M. ozzardi dans les
forêts semi caduques. En conséquence, deux types de transmission
sont suggérés : M. ozzardi-Simulium et M. persistans-Culicoides.
KEY WORDS : mansonelliasis, Venezuela, distribution, vegetation types.
MOTS CLES : mansonelloses, Venezuela, distribution, végétation.
INTRODUCTION
M
ansonelliases are e n d e m i c in several regions
of Africa, the Caribbean and Latin America. In
South America it has b e e n reported in V e n e zuela, Colombia, Brazil, Guyana, Suriname, Argentina
a n d Peru (Sasa, 1976; Hawking, 1979), although in
most o f these countries its prevalence and geographical
distribution, as well as the environmental factors determining distribution, have yet to b e defined. However,
many o f the areas in South America w h e r e mansonelliases are e n d e m i c lie within the Amazon basin
( K o z e k et al., 1 9 8 2 b ) .
* Centro Amazonico para la Investigación y Control de Enfermedades
Tropicales (CAICET), Ave. Perimetral, Pto. Ayacucho, Edo. Amazonas,
Venezuela.
** Instituto de Zoología Tropical, Facultad de Ciencias, Universidad
Central de Venezuela, P.O. Box 47058, Caracas 1041A, Venezuela.
Correspondence: R. Guerrero.
Tel.: (582)-372-5187 - Fax: (582)-605-1204.
Email: rguerrer@strix.ciens.ucv.ve
Parasite, 2 0 0 0 , 7, 7 1 - 7 6
In Amazonas State in Venezuela, it has b e e n reported
that Mansonella
(Mansonella)
ozzardi (Manson, 1 8 9 7 )
and Mansonella
(Esslingeria)
perstans
(Manson, 1 8 9 1 )
mainly affect the ethnic groups that inhabit the region
(Baumgartner, 1955; B e a v e r et al, 1976; Botto et al,
1983; Formica & Botto, 1990).
T h e s e studies s h o w that mansonelliases are widely distributed throughout Amazonas State. However, with the
e x c e p t i o n s o f Botto et al. ( 1 9 8 3 ) and Formica & Botto
( 1 9 9 0 ) , they underestimate the infected population
b e c a u s e the diagnostic techniques used w e r e not very
sensitive. Thus there is a n e e d to evaluate the real
situation o f these filarial parasites b y m e a n s o f a technique o f proven sensitivity, such as the Knott technique
( B o t t o et al, 1983; Raccurt et al, 1982).
Likewise, there have not b e e n any studies which correlate the distribution o f these parasites, along with epidemiological indexes such as prevalence and parasitical load, to environmental factors like vegetation and
rainfall a m o n g others.
For this reason w e have carried out studies in different parts o f Amazonas State in Venezuela and in o n e
Mémoire
71
GÓMEZ J . & GUERRERO R.
locality in Bolívar State in order to determine the prevalence, parasitical load and precise t a x o n o m i c identity o f the Mansonella
species involved, and the characteristics o f the different regions in terms o f their
vegetation, precipitation and altitude, with the aim o f
contributing to the framework o f current k n o w l e d g e
about these parasites in the areas in question.
I - Upper Cuao, midstream ( n o climatological station,
so the figures for G are used).
J - River Parguaza, downstream in Bolivar State (27.03° C,
100 m ) .
K - T h e T o p o c h o stream, close to Parhueña village
( 2 7 . 0 3 ° C , 100 m ) .
MATERIALS AND METHODS
AREA OF STUDY
T
his mainly comprises Amazonas State, with o n e
adjacent locality in Bolivar State.
T h e Amazonas State is located in the south o f
Venezuela and has an area o f 175,750 square kilometres. It lies in the basin o f the O r i n o c o and Negro
rivers, upstream from the c o n v e r g e n c e o f the O r i n o c o
a n d Meta rivers, o n the frontier with Brazil a n d
Colombia.
This region is characterised by high average temperatures, abundant and persistent rain, high relative humidity and an extraordinary variety o f vegetation, especially o f the forestal type. M a x i m u m precipitation
occurs in the south-west o f the state, while the driest
parts are in the south-east and north-west.
It has b e e n estimated that 93 % o f the region is covered
b y forest with two to four layers o f vegetation, the
lower levels consisting o f shrubbery and the upper
levels o f big trees. T h e rest o f the surface (7 % ) c o m prises savannahs, rivers and rocky outcrops ( B o a d a ,
1983).
T h e samples w e r e collected from 17 localities distributed in 11 areas characterised according to their vegetation, following Huber ( 1 9 8 2 ) . T h e annual mean rainfall and annual mean temperatures given are calculated
from figures provided by the Direction o f Hidrology
and M e t e o r o l o g y at the V e n e z u e l a n E n v i r o n m e n t
Ministry.
T h e areas are as follows (Fig. 1):
A - Rivers Temi and Atacavi, at the source o f the Atab a p o river (26.74°C, 100 metres a b o v e sea level).
B - Upper Orinoco, above the village of O c a m o (26.75°C,
150 m ) .
C - Cejal, between La Esmeralda and Tama-Tama (27.02°C,
100 m ) .
D - River Cunucunuma, between Tama-Tama and Culebra ( 2 7 . 0 2 ° C , 2 2 0 m ) .
E - Isla Ratón, an island in the O r i n o c o river south o f
Puerto A y a c u c h o (27.03° C, 100 m ) .
F - River Cataniapo, downstream ( 2 7 . 0 3 ° C , 100 m ) .
G - Rivers Cuao, Sipapo and Autana, downstream and
river mouths ( 2 7 . 2 4 ° C , 100 m ) .
H - Upper Ventuari, the head o f the river a b o v e Cacuri
(27.68°C, 500 m).
72
Mémoire
Fig. 1. - R e g i o n s w h e r e t h e study w a s c a r r i e d out.
A ) T e m i - A t a c a v i rivers. B ) U p p e r O r i n o c o . C ) Cejal. D ) C u n u c u n u m a
river. E ) Isla R a t o n . F ) C a t a n i a p o river. G ) C u a o , S i p a p o , a n d Atitana
rivers. H ) U p p e r Ventuari.
I) Upper Cuao. J ) Parguaza
river.
K) T o p o c h o stream.
T h e localities and their environmental characteristics
are presented in T a b l e I. T h e human population studied comprised ethnic groups inhabiting the regions,
p r i n c i p a l l y Y a n o m a m i s ( o n the U p p e r O r i n o c o ) ,
Y e k u a n a s ( o n the Upper Ventuari and River Cunucunuma), Curripacos, Banivas and Piapocos ( o n the Temi
and Atacavi rivers), and Piaroas and Guajibos ( o n the
Cuao, Sipapo, Autana, Cataniapo and Parguaza rivers
and Isla Raton).
PARASITOLOGICAL METHODS
A b l o o d sample o f 1.0 ml was taken from e a c h person
and processed by the Knott technique. T h e c o m p l e t e
t u b e w a s then e x a m i n e d , using a ZEISS Standard
microscope with lOx and 4 0 x magnification. T h e cases
that tested positively for microfilariae were then stained
with Mayer's haematoxylin, following the technique
described by D e n h a m ( 1 9 7 5 ) , and their morphological
Parasite, 2 0 0 0 , 7, 7 1 - 7 6
M A N S O N E L U A S E S IN S O U T H E R N V E N E Z U E L A
Localities
Region
Precipitation
Rio Temi-Rio Atacavi
Alto Rio Ocamo
Mavaca-Rio Orinoco
Ocamo-Rio Orinoco
Platanal-Rio Orinoco
Rio Mavaca
Cejal-Rio Orinoco
Rio Cunucunuma
Isla Raton
Rio Cataniapo
Rio Autana
Rio Cuao
Rio Sipapo
Alto Rio Ventuari
Alto Rio Cuao
Rio Parguaza
Caiio Topocho
A
В
в
в
в
в
с
D
E
F
G
G
G
H
I
J
К
3,574
2,607
2,479
2,607
2,479
2,479
2,632
3,128
2,183
2,571
2,533
2,533
2,533
2,495
2,533
2,737
2,448
1
1
Vegetation
Transition amazonian Caatinga/Low lands Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest
Montainous and basimontainous Pluvial Forest
Savannah with Riverside Forest
Rocky Semideciduous Forest alisio type
Low lands Pluvial Forest with bush
Low lands Pluvial Forest with bush
Low lands Pluvial Forest with bush
Semideciduous Forest alisio type
Montainous and basimontainous Pluvial Forest
Montainous and basimontainous Pluvial Forest
Rocky Semideciduous Forest alisio type
Annual mean (in mm.).
Table I. - Environmental characteristic in the studied localities.
characters w e r e e x a m i n e d for the purposes o f taxon o m i c identification, using 4 0 x and lOOx objectives.
QUANTITATIVE METHODS
The quantitative tenninology and criteria used are those
defined by Kisielewska ( 1 9 7 0 ) and modified by Guer­
rero ( 1 9 7 9 , 1 9 9 6 ) , as follows:
. Prevalence: percentage o f infected hosts.
. Relative density: average number o f parasites per
infected host.
. Absolute density: average n u m b e r o f parasites per
host (infected and uninfected).
. Multiple infection: percentage o f hosts infected by
m o r e than o n e species o f parasite.
. Infection index: a combination o f prevalence and
absolute density, permitting the determination o f the
degree o f infection o f the human groups and regions
studied.
It is important to point out here that s o m e authors
favour the use o f the geometric mean in order to deter­
mine parasitic load (density) instead o f the arithmeticmean (Brandling-Bennett et al, 1 9 8 1 ; Marshall et al.,
1974; Sasa, 1 9 7 6 ) . H o w e v e r , the arithmetic m e a n ,
which is e m p l o y e d in the present work, remains a
useful measure that provides valid information in the
study o f filariasis (Sasa, 1976), strictly following the cri­
teria laid d o w n by Kisielewska (op. ciO and Guerrero
(op.
cit.).
STATISTICAL ANALYSIS
For the statistical analysis b e t w e e n the quantitative
parameters (Prevalence, both densities and infection
index) and rainfall and altitude, the product-moment
correlation coefficient (Coefficient for Pearson's corrParasite, 2 0 0 0 ,
7,
71-76
relation) was calculated following the procedure des­
cribed by Sokal & Rohlf ( 1 9 6 9 ) , with data processing
carried out by the statistical programme Statgraphics
Version 4.0 Co.
RESULTS
I
n the samples collected from 1,057 inhabitants o f
17 localities, total prevalence was 18.54 %. 11.26 %
w e r e parasited by Mansonella
perstans,
9.93 % by
Mansonella
ozzardi
and 2.63 % by both species. T h e
average o f microfilaremia was 4 8 . 1 9 mf/mL o f b l o o d
in M. perstans
and 13-79 mf,mL in M.
ozzardi.
M. ozzardi
was found in 12 ( 7 0 . 6 % ) o f the 17 ana­
lysed localities, and M. perstans
in eight (47.1 % ) . In
five localities (29.41 % ) both species were found, while
two localities (the Cunucunuma and Mavaca rivers) were
free o f mansonelliasis. T h e prevalence was very high
in s o m e localities, especially Alto Ventuari ( 7 1 . 2 1 ) for
M. ozzardi
and the T e m i and Atacavi rivers ( 8 8 . 1 6 % )
for M. perstans
(Table II).
The number o f circulating microfilariae was low. G e n e ­
rally speaking, in localities where microfilarial density
was high the prevalence rate was also high, resulting
in an elevated infection index. However, n o relation
was found b e t w e e n the infection index and multiple
infection.
T h e coefficient for Pearson's correlation shows statis­
tically significant correlations b e t w e e n the quantitative
parameters and total average rainfall in the localities
studied in the case o f M. perstans,
and altitude in the
case o f M.
ozzardi.
Major differences were found in the distribution o f both
species o f Mansonella
in relation to type o f vegetation.
Mémoire
73
GÓMEZ J . & GUERRERO R.
Localities
Prevalence
Number
%
of
M. o.
M. p.
cases
Río Temi-Río Atacavi
Alto Río Ocamo
Mavaca-Río Orinoco
Ocamo-Río Orinoco
Platanal-Río Orinoco
Río Mavaca
Ce¡al-Río Orinoco
Río Cunucunuma
Isla Raton
Río Cataniapo
Río Autana
Río Cuao
Río Sipapo
Alto Río Vcntuari
Alto Río Cuao
Río Parguaza
Caño Topocho
1
2
1
76
38
82
35
47
66
30
82
60
119
8
50
27
66
67
170
34
1
13.2
7.9
18.3
5.7
14.9
0.0
3.3
0.0
3.3
2.52
88.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
17.7
12.5
12.5
2.0
0.0
71.2
19.4
0.0
0.0
4.0
3.7
0.0
31.3
2.4
5.9
Density (mf/mL)
Absolute
Infection index
Relative
M. o.
M.p.
M. o.
M.p.
1.91
7.0
1i
4.2
2.3
0.0
0.4
0.0
5.4
0.7
4.3
0. 1
0.0
193.9
6.9
0.0
0.0
467.3
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
39.6
1.0
1.5
0.6
0.0
150.4
2.7
2.1
14.5
88.0
12.9
73.5
15.1
0.0
13.0
0.0
162.5
29.3
34.0
3.0
0.0
272.3
35.4
0.0
0.0
530.1
0.0
0.0
0.0
o.o
o.o
0.0
0.0
O.o
224.4
8.0
37.0
15.0
0.0
479.8
116.5
36.0
M. o.
0.3
0.6
0.4
0.2
".3
0.0
0.1
0.0
0.2
0.1
0.5
0.002
0.0
138.1
1.3
0.0
0.0
M.p.
411.9
0.0
0.0
o.o
o.o
0.0
0.0
0.0
0.0
".o
0.1
0.1
0.1
0.0
47.1
0.1
0.1
Multiple
infection
13.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
2.5
12.5
2.0
o.o
0.0
19.4
0.0
0.0
Mansonella ozzardi.
Mansonella perstans.
Table II. - Quantitative results in the studied localities.
Criteria
Prevalence M. ozzardi
Prevalence M. perstans
Absolute density M. ozzardi
Absolute density M. perstans
Relative density M. ozzardi
Relative density M. perstans
Infection index M. ozzardi
Infection index M. perstans
Precipitation
Altitude
- 0.6930
(0.792)
0.7233
(O.OOD*
- 0.1169
(0.655)
0.7518
(O.OOD*
- 0.2953
(0.250)
0.5479
(0.023)
- 0.1064
(0.685)
0.7916
(0.000)*
0.897
(0.000)*
- 0.140
(0.591)
0.923
(0.000)*
- 0.093
(0.723)
0.717
(0.001)*
- 0.082
(0.754)
0.921
(0.000)*
- 0.113
(0.666)
* Correlation (P = 0.001).
Table III. - Pearson's correlation coefficients between quantitative
criteria and environmental variables.
M. ozzardi evidences a higher infection index in those
regions which have Alisio-type semi-deciduous forest,
while M. perstans is higher in Amazonian caatinga transition in pluvial lowland forest.
DISCUSSION
T
he results o f this study confirm that mansonelliases is widespread in Amazonas State a n d the
neighbouring areas o f Bolivar State, in the south
o f Venezuela.
74
T h e main focuses are in the regions o f the T e m i a n d
Atacavi rivers with an infection index (i.i.) o f 413-52,
and in Upper Ventuari (i.i. = 1 3 8 . 0 9 ) .
The former undoubtedly represents an extension o f the
focus described b y Formica & Botto ( 1 9 9 0 ) in V e n e zuela and K o z e k et al. ( 1 9 8 2 a ) in Colombia, a focus
in which M. perstans must b e e n d e m i c . Apart from the
d o m i n a n c e o f M. perstans,
this focus is characterised
by high prevalence and an elevated percentage o f inhabitants parasited b y both species o f Mansonella.
T h e Upper Ventuari focus is probably an extension o f
the o n e described by G o d o y et al. ( 1 9 8 0 ) in the southwest o f Bolivar State, and is due to M.
ozzardi.
Lesser infestations o c c u r in the regions o f the Upper
Cuao (i.i. = 4 9 . 3 3 ) and River Cataniapo (i.i. = 7.12). Both
of these regions w e r e reported as focuses o f m a n s o nelliasis by Baumgartner ( 1 9 5 5 ) . T h e remaining localities studied had infection indexes o f less than o n e (1.0).
M. ozzardi w a s spread over a wider area than M. perstans, the latter being distributed in the north-west o f
Amazonas State, from the T e m i a n d Atacavi rivers to
north o f Puerto Ayacucho, o n the Cuao, Sipapo and
Autana rivers, and in neighbouring localities in Bolivar
State.
M. ozzardi
is found to the east a n d south-east o f the
Temi a n d Atacavi rivers as far as the Upper O r i n o c o ,
and in the regions near to the mouth o f the Casiquiare
river, w h e r e mansonelliasis has previously b e e n reported ( B e a v e r et al, 1 9 7 6 ) .
Overlapping o f both species, a n d consequently multiple infection, occurs in the regions o f the Temi, Atacavi, Autana, Cuao a n d Cataniapo rivers.
Mémoire
Parasite, 2 0 0 0 , 7, 7 1 - 7 6
MANSONELLIASES IN SOUTHERN VENEZUELA
M. ozzardi
Vegetation types
Transition amazonian Caatinga/Low lands
Pluvial Forest
Low lands Pluvial Forest
Low lands Pluvial Forest with bush
Mountainous and basimountainous Pluvial
Forest
Rocky semideciduous Forest alisio type
Savannah with Riverside Forest
Semideciduous Forest alisio type
1
2
Prevalence
A. den.
1
M. perstans
Inf. Ind.
2
Prevalence
A. den.
Inf. ind.
13.16
1.91
0.25
88.16
467.29
411.29
9.40
2.35
4.08
2.43
0.44
1.44
0.23
0.01
0.06
0.00
4.71
7.84
0.00
1.14
33.04
0.00
0.05
2.59
1.96
3.33
71.21
0.58
5.42
193.91
0.01
0.18
138.08
15.03
0.00
0.00
31.27
0.00
0.00
4.70
0.00
0.00
Absolute density.
Infection Index.
Table IV. — Values of qualitative criteria of Mansonella spp. according with the types of vegetation.
T h e quantitative criteria o f prevalence, absolute den­
sity and infection index calculated for M. perstans
evi­
d e n c e d a high correlation to precipitation in e a c h
locality, rainfall being the most influential environ­
mental variable for the transmission o f this species. This
is probably due to the conditions required b y the
vector: in relative humidity or continuous rain, seasonal
effects are eliminated, which produces a more efficient,
ongoing transmission o f the filaria.
In the c a s e o f M. ozzardi
the correlation is with alti­
tude: in other words, the most effective vectors for
transmitting this s p e c i e s are found in localities in
higher regions.
With respect to types o f vegetation, transmission o f
M. perstans
is most favoured b y Amazonian caatinga
transition in lowland pluvial forest, while M.
ozzardi
is favoured b y alisio-type semi-deciduous forest.
T h e s e results confirm that the two species o f Manso­
nella require different environmental conditions for
their transmission, and probably have different vectors
in natural conditions.
Laboratory studies reveal that Culicoides spp. and Simulium spp. can act as vectors for M. ozzardi
(Tidwell
& Tidwell, 1 9 8 2 ) . In natural conditions it is likely that
Simulium
is the vector for M. ozzardi
and
Culicoides
for M. perstans.
It is supported by field observations,
in localities with d o m i n a n c e o f M. ozzardi,
species o f
Simulium w e r e abundant and in localities with domi­
n a n c e o f M. perstans,
Culicoides
ever w e r e present.
Larvae and pupae o f Simulidae need fast runing waters
(Wygodzinsky & Coscaron, 1 9 8 9 ) as usually are in loca­
lities in higher regions w e r e M. ozzardi
is dominant.
In conclusion, mansonelliases is widespread in Amazonas State, the main focuses in the localities studied
being situated o n the Temi and Atacavi rivers and the
Upper Ventuari, with M. ozzardi
having a wider dis­
tribution than M. perstans. T h e latter species evidences
a greater transmission rate in areas o f higher rainfall,
Parasite, 2 0 0 0 , 7, 7 1 - 7 6
while the transmission o f M. ozzardi
is favoured b y
higher altitude. T h e two species also evidence diffe­
rent transmission rates with respect to the types o f
vegetation studied, probably b e c a u s e the respective
types o f vegetation favour the development o f the cor­
responding vectors for these filariae.
ACKNOWLEDGEMENTS
W
e would like to thank Miguel Conde, Mayila
Garcia and Manuel Bolivar for their help in
the laboratory and with field work; Carlos
Noguera for his advice and suggestions; Dr Carlos
Botto for his support in the last stages o f this work;
and Tibisay Rangel for her help and collaboration at
all times. This research received financial support from
the Consejo Nacional de Investigaciones Científicas y
T e c n o l ó g i c a s ( C O N O C I T ) o f Venezuela, through grant
no. S l - 2 0 1 4 .
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