Acta Tropica 153 (2016) 16

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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica

Mansonella ozzardi in Neotropical region of Argentina: Prevalence

through time (19862010)
Cecilia A. Veggiani Aybar a,b, , Mara J. Dantur Juri a,b , Mario O. Zaidenberg c
a
Instituto Superior de Entomologa Dr. Abraham Willink, Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumn, 4000
Tucumn, Argentina
b
Consejo Nacional de Investigaciones Cientcas y Tcnicas, 4000 Tucumn, Argentina
c
Coordinacin Nacional de Control de Vectores, Ministerio de Salud de la Nacin, 4400 Salta, Argentina

a r t i c l e

i n f o

Article history:
Received 30 April 2015
Received in revised form 4 September 2015
Accepted 27 September 2015
Available online 1 October 2015
Keywords:
Mansonelliasis
Epidemiology
Subtropical mountainous rainforest
Northwestern Argentina

a b s t r a c t
Human lariasis caused by Mansonella ozzardi is a parasitic infection of a controversial pathology and
poorly studied in Argentina. The aim of this study was not only to obtain data of the prevalence of
M. ozzardi in Northwestern Argentina through comparison of infection rates in relation to sex and age
group determining the range of distribution of mansonelliasis in the region but also to investigate the
prevalence of the cases over time. Through eld work carried between 1986 and 2010 by technicians of the
National Ministry of Health, aiming to detect active cases of malaria in the Northwestern Argentina, blood
samples were taken for smear and thick blood. 417 blood samples were examined, 381 of them (91.4%)
were positive for M. ozzardi. The highest prevalence was found in Salta province (92.3%) mainly affecting
the male sex (92.6%) and the age groups comprised between 4857 years (97.0%) and 68 (90.7%).
The paired t-test and Spearman coefcients showed signicant differences in prevalence according to
sex (t = 2.677; p = 0.015), and according infection rates in males and females/age (r = 0.994; p = 0.001;
r = 0.994, p = 0.001, respectively). The prevalence over time showed a general pattern with the highest
cases in 1986, decreasing later during the following years. Aguas Blancas, El Oculto and San Ramn de
la Nueva Orn, exhibited a pattern of prevalence according to the general trend but Salvador Mazza and
Tartagal, which are also localities close to the border with Bolivia, showed peaks of cases up to 2010.
These results provide relevant information about M. ozzardi in Argentina, demonstrating not only its
presence and endemicity after almost 100 years from its discovery in the country, but also its wide range
of distribution in the region.
2015 Elsevier B.V. All rights reserved.

1. Introduction
Mansonella ozzardi (Nematoda: Onchocercidae) is a larial parasite which inhabits serous cavities of human hosts and that
generally are found accidentally when patients with symptoms of
malaria visit the physician and thick and thin blood smears reveal
the presence of larval forms of the nematodes called microlariae
(Formica and Botto,1990; Nathan and Stroom, 1991). At present,
this parasite is distributed in America, represented in Argentina,
Bolivia, Brazil, Colombia, the Caribbean, Mexico, Panama, Peru and
Venezuela (Tavares and Fraiha Neto, 1997; Shelley and Coscaron,
2001; Arrspide et al., 2012).

Corresponding author. Tel.: +54 381 4232965; fax: +54 381 4232965.
E-mail address: ceciliaveggianiaybar@yahoo.com.ar (C.A. Veggiani Aybar).
http://dx.doi.org/10.1016/j.actatropica.2015.09.018
0001-706X/ 2015 Elsevier B.V. All rights reserved.

Mansonella ozzardi is transmitted through the bite of

haematophagous diptera families, Ceratopogonidae (Culicoides)
and Simuliidae (Simulium) (Shelley and Coscaron, 2001). In
Argentina, transmission is related to biting midges, Culicoides
lahillei (main vector) and Culicoides paraensis (secondary vector),
and black ies Simulium exiguum (secondary vector) (Shelley
and Coscaron, 2001). Although human infection by M. ozzardi is
considered a relatively non-pathogenic, some authors described
symptoms that include fever, joint pains, headache, pruritic skin
eruptions, coldness in the legs, erythematous and itchy papules,
lymphadenopathy, high eosinophilia, pulmonary symptoms and
occurrence of visual lesions, which in turn can lead to blindness
(Tavares and Fraiha Neto, 1997; Batista et al., 1960; Branco et al.,
1998; Loja Oropeza et al., 1999; Bartoloni et al., 1999; Vianna et al.,
2012). However, the pathogenicity is still a controversial subject
requiring further study (Medrano et al., 1992; Medeiros et al.,
2009).

C.A. Veggiani Aybar et al. / Acta Tropica 153 (2016) 16

The presence of microlariae infection in Argentina was recognized by malaria surveys in the Northwestern region of the
country, with the species Microlaria tucumana described by Aroz
and Biglieri (1915) in Tucumn province, a homonym of Mansonella ozzardi (Davis, 1928). This nding marked the beginning of a
series of epidemiological investigation in Northwestern Argentina
(Padilla, 1915; Rosenbsch, 1915; Mhlens et al., 1925; Davis,
and Wygodzinsky, 1950; Taranto and Castelli, 1988;
1928; Romana
Minoprio et al., 1988; Remondegui et al., 1988; Jrg, 1993; Zrate,
1996; Zaidenberg, 1997; Guzmn et al., 1998; Socolsky, 2010;
Degese et al., 2012). Since its discovery in the country, almost 100
years later, its existence is still reported, although sporadically, and
the epidemiology of this disease is still poorly understood, partly
because it occurs almost exclusively in areas with specic microclimate but also by their scarce attention in public health.
For the reasons exposed above, the aim of this investigation was
to obtain data of human infection by M. ozzardi in Northwestern
Argentina through comparison of infection rates in relation to sex
and age group, in order to determine the prevalence and the range
of distribution of mansonelliasis in the region. Also, the prevalence
over time was considered important to investigate and lastly, were
sought to identify the potential vectors involved in the transmission
of M. ozzardi.
2. Methods
2.1. Study area
This study was performed in two patches, central and northern,
of the subtropical mountainous rainforest of Argentina, also known
as Yungas. Yungas cover an area of 56,000 km2 , from the Bolivian
border (23 S) to the north of the Catamarca province (29 S), passing
through Salta, Jujuy and Tucumn provinces.
The climate of this forested region is subtropical with a dry
season, with the average of annual temperature of 1820 C
and marked seasonality of rainfall. The rainfall has a monsoon
regime resulting in rainy summers and dry winters, and with
90% of the rainfall events occurring during 4 moths in the year
(December, January, February and March). Along its altitudinal gradient (4002300 m.a.s.l), the tree species turnover promotes the
occurrence of three altitudinal belts, pre-montane forest, (400900
m.a.s.l), lower montane forest (900-1600 m.a.s.l) and upper montane forest (16002300 m.a.s.l).

the Manual de Normas y Procedimientos de Vigilancia y Control de

Enfermedades de Noticacin Obligatoria.
2.4. Parasitological studies
Assessment of M. ozzardi prevalence is performed using thick
and thin blood smears obtained by digital puncture of 417 volunteers. The blood samples were placed on slide, air-drying and
dehaemoglobinised in methylene blue. Subsequently, the blood
samples were stained with Giemsa 10% and examined with a
binocular microscope with an immersion lens of 1000 (100) for
microlariae identication following WHO (1997) and Post et al.
(2003). It was observed morphological characters as cephalic and
caudal space, pattern of nucleation of the tail and tail shape to
identify the microlariae. The diagnosis was conrmed by technician experts from Coordinacin Nacional de Control de Vectores,
Delegacin Salta.
In turn, experimental studies were performed with specimens
of the genus Culicoides collected at several localities of the Yungas.
Biting midges were identied at specic level following Spinelli
et al. (2005) and they were stained with acid haematoxylin, dissected into three parts (head, thorax and abdomen) and placed on
a slide with a drop of glycerine for examined under a microscope
(Yazarbal et al., 1985).
2.5. Data analysis
Prevalence data of individuals infected were evaluated according to the sex, age group and provenance (province and locality).
A paired t-test was applied to determine whether there were
signicant differences in prevalence according to sex, and Spearman correlation coefcient to determine if the prevalence both in
female and men was related to age group. Statistical analysis was
performed using Statistica 6.0 (Statsoft, 2001). The variables that
contributed least to the explanation of the models were eliminated
taking statistical signicance (p < 0.05) into consideration.
In turn, a descriptive analysis of the prevalence over time based
on the temporal uctuation of positive cases of M. ozzardi registered
during 19862010 in Northwestern Argentina was carried out in
order to determine not only a general trend but also by grouping
the closest localities, potential different patterns.
3. Results

2.2. Population study

Based on the eld work carried out between 1986 and 2010
by the technicians from National Ministry of Health for detecting active cases of malaria, blood samples in 18 localities were
taken, 13 in Salta province and ve in Jujuy province, Northwestern
Argentina (Fig. 1).
In these areas, the inhabitants live in scattered communities
and near riverside, and the local economy is based on agriculture
(crops mainly sugarcane, snuff and soybeans), native wood extraction (Podocarpus and Cedrela) and exotic species (Eucalyptus and
Pinus), and to a lesser extent the rearing of livestock (bovine and
ovine).
2.3. Ethical considerations
The study methodology, including the ethical aspects, was
approved by the Ministry of Health of Argentina, which has an Ethical Committee who revised these aspects. The blood samples were
obtained by trained technicians from Coordinacin Nacional de
Control de Vectores, following the standardized protocol approved
by the Ministry of Health of Argentina. This Protocol is included in

The presence of microlariae was detected in 381 (91.4%) blood

lms of a total of 417 samples observed (Fig. 2), being 97.1% identied as Mansonella ozzardi and the remaining 2.9% as unknown.
The highest prevalence rates were found in Salta province
(92.3%) compared to Jujuy province (85.9%) (Table 1). In Salta
province, Tartagal exhibited 46.9% of positive samples meanwhile
in San Ramn de la Nueva Orn it was observed 30.1%. In Jujuy
province, 56.4% presented blood microlariae of M. ozzardi in Libertador General San Martn and 20% it was observed in San Pedro
de Jujuy.
Furthermore, M. ozzardi is reported for the rst time in the
localities of Acambuco, Aguas Blancas, Algarrobal, Pichanal, Embarcacin, General Ballivian, General Mosconi, Aguaray and Campo
Durn, in Salta province; and Palma Sola, San Borja, San Pedro de
Jujuy and Libertador General San Martn, in Jujuy province, expanding its range of distribution in Northwestern Argentina. On the
other hand, a 2.4% prevalence of infected individuals from Bolivia
was also registered.
Mansonella ozzardi infections were generally more prevalent
among males (92.6%) with respect to females (88.7%), which were
also observed according to location of provenance of individuals

C.A. Veggiani Aybar et al. / Acta Tropica 153 (2016) 16

Fig. 1. Geographical distribution of the localities in Salta and Jujuy provinces, Northwestern Argentina (1Acambuco, 2Aguas Blancas, 3El Oculto, 4San Ramn de
la Nueva Orn, 5Algarrobal, 6Pichanal, 7Embarcacin, 8General Ballivian, 9General Mosconi, 10Tartagal, 11Aguaray, 12Campo Durn, 13Salvador Mazza,
14Palma Sola, 15Isla Chica, 16San Borja, 17San Pedro de Jujuy and 18Libertador General San Martn).

infected. Prevalence was highest among individuals of 4857 years

(97.0%) and 68 (90.7%) (Fig. 3).
The paired t-test determined signicant differences between
males and females infected (t = 2.677; df = 18; p < 0.015). Infection
rate in males and females was also positively associated with
age (Spearman coefcient r = 0.994, p < 0.001; r = 0.994, p < 0.001,
respectively).
The prevalence over time showed that the highest cases
occurred in 1986, starting to decrease since then, with minor peaks
in 1988, 1991, 1995 and 1998 (Fig. 4).

Considering the localities grouped by their proximity, Aguas

Blancas, El Oculto and San Ramn de la Nueva Orn, which are near
to one of the border with Bolivia, exhibited a pattern of prevalence
over time according to the general trend with the highest prevalence since 1986 until 1989, and decreasing during the following
years. The pattern observed at Salvador Mazza and Tartagal, which
are also near to the other border with Bolivia, was totally different, showing peaks of cases up to 2010. Minor quantities of cases
were observed at Pichanal, Embarcacin and Algarrobal, following
the general trend. A different situation was observed at San Pedro

Table 1
Number of individuals examined/positive for Mansonella ozzardi by sex in localities situated throughout the Yungas.
Localities

Positive/Examined (Prevalence %)

Salta Province
Acambuco
Aguas Blancas
El Oculto
San Ramn de la Nueva Orn
Algarrobal
Pichanal
Embarcacin
General Ballivian
General Mosconi
Tartagal
Aguaray
Campo Durn
Salvador Mazza
Total

Males
8/10 (80.0)
7/9 (77.7)
9/10 (90.0)
75/79 (94.9)
4/5 (80.0)
6/6 (100.0)
4/4 (100.0)
2/2 (100.0)
3/3 (100.0)
91/97 (93.8)
3/3 (100.0)
3/3 (100.0)
7/9 (77.8)
222/240 (92.5)

Females
3/4 (75.0)
2/2 (100.0)
3/3 (100.0)
23/25 (92.0)
1/2 (50.0)
1/1 (100.0)
2/2 (100.0)
1/1 (100.0)
1/1 (100.0)
62/64 (96.9)
2/3 (66.7)
1/1 (100.0)
2/4 (50.0)
104/113 (92.0)

Total
11/14 (78.6)
9/11 (81.8)
12/13 (92.3)
98/104 (94.2)
5/7 (71.4)
7/7 (100.0)
6/6 (100.0)
3/3 (100.0)
4/4 (100.0)
153/161 (95.0)
5/6 (83.3)
4/4 (100.0)
9/13 (69.2)
326/353 (92.3)

Jujuy Province
Palma Sola
Isla Chica
San Borja
San Pedro de Jujuy
Libertador General San Martn
Total

3/3 (100.0)
4/4 (100.0)
3/4 (75.0)
9/11 (81.8)
22/22 (100.0)
41/44 (93.2)

1/3 (33.3)
1/1 (100.0)
1/2 (50.0)
2/4 (50.0)
9/10 (90.0)
14/20 (70.0)

4/6 (66.7)
5/5 (100.0)
4/6 (66.7)
11/15 (73.3)
31/32 (96.9)
55/64 (85.9)

C.A. Veggiani Aybar et al. / Acta Tropica 153 (2016) 16

Fig. 4. General trend showing the temporal uctuation of positive cases to M.

ozzardi, in Northwestern Argentina, during 19862010.

Fig. 2. Giemsa-stained microlarias of M. ozzardi isolated from of volunteers (100).

Source: photomicrography of the author.

de Jujuy and Libertador General San Martn, where the prevalence

over time was longer with cases since 1988 up to 2010 (Fig. 5).
Experimental studies with the vectors revealed the presence of
M. ozzardi in four of the 18 dissected specimens. Culicoides lahillei, C.
debilipalpis and C. paraensis were the infected species, and Sargento
Moya (Tucumn province), El Oculto (Salta province), Libertador
General San Martn (Jujuy province), and Pozo del Bermejo (Bolivia)
are the localities were these specimens were collected.
4. Discussion
Mansonella ozzardi is a parasite which has showed a high prevalence in populations of tropical areas, varying the infection rate
from place to another and according to the diagnosis method used
and the concentration of microlariae. In the present investigation,
M. ozzardi was found in all localities studied, with prevalence of
91.4% (381/417 infected individuals), and with a higher infection
rate in Salta province. The prevalence was greater in males than
females and increased with age, independent of sex. Similar results
were reported in previous studies performed in Northwestern
Argentina (Mhlens et al., 1925; Remondegui et al., 1988; Zrate,

1996; Zaidenberg, 1997) and in other countries (Shelley, 1975;

Botero and Restrepo, 2003; Martins et al., 2010). Some authors
attribute that this behavior could be related to the type of the
environment and the activities performed for the individuals. So,
it has been observed that in rural areas both females and males
involved in agriculture activities presented similar infection rates.
Furthermore, individuals with their dwellings close to the rivers
and working in the eld, results much more exposed to the bites
of the vectors, and therefore, at a greater risk of infection (Shelley,
1975; Botero and Restrepo, 2003; Martins et al., 2010).
In turn, a higher prevalence of older adults infected is reported in
the present research, as well as it had also been registered in urban
areas in previous reports, suggesting that these individuals could
present a series of continuous overlaps, keeping the untreated
infections during their life (Botero and Restrepo, 2003; Medeiros
et al., 2008).
The prevalence over time showed that the highest cases
occurred in 1986, starting to decrease up today. The localities studied were endemic areas to malaria disease, therefore was not rare
to nd this microlaria during the eld work by the searching
of people sick with Plasmodium parasites (Arrspide et al., 2009;
Dantur Juri et al., 2013). Localities near the border with Bolivia
showed different patterns. Aguas Blancas, El Oculto and San Ramn
de la Nueva Orn presented prevalence over time according to the

Fig. 3. Prevalence of M. ozzardi infections according to the age group, from 1986 to 2010, in Northwestern Argentina.

C.A. Veggiani Aybar et al. / Acta Tropica 153 (2016) 16

Fig. 5. Temporal uctuation of positive cases to M. ozzardi in localities grouped by their proximity.

general trend, with the highest cases at 19861989, meanwhile Salvador Mazza and Tartagal have shown peaks of cases up to 2010.
In Jujuy localities, San Pedro de Jujuy and Libertador General San
Martn, it was observed the prevalence over time with cases since
1988 up to 2010.
Taking into consideration previous studies to compare with,
Mhlens et al. (1925) and Remondegui et al. (1988) has reported
in Jujuy province a prevalence between 39.1% and 41.1%, respectively. Later, Zrate (1996) and Zaidenberg (1997) has cited in Salta
province, a prevalence of 50%. Considering our results, it can be
said that the values observed in this study agree with the high
prevalence of this parasitism for the region. Furthermore, in other
countries as Bolivia, Brazil and Peru have also been reported similar prevalence values (Medrano et al., 1992; Bartoloni et al., 1999;
Medeiros et al., 2009; Arrspide et al., 2012), which also conrming
the high endemicity observed in the present investigation.
Also, the migration of infected individuals in job search may
be responsible of the establishing of new active M. ozzardi transmission foci, because the vector species have a wide geographic
distribution in Argentina; the latter may also explain the observed
in the present study. Lastly, it is probable that the prevalence in this
region is due to social and environmental factors, considering the
lack of a continuous and wide-ranging treatment program.
Another result has been the detection in 11 blood samples of
microlariae that differ of M. ozzardi by the length and arrangement
of nuclei in the cephalic space.
Finally, experimental studies in specimens of Culicoides revealed
the presence of M. ozzardi in endemics areas of Northwestern
Argentina. However, is necessary to continue with these studies
and to determine the Parasitic Infection Rates (PIR) in the specimens collected in the region.
5. Conclusions
This study determined high rates of M. ozzardi infection in
Argentina during period 19862010, highlighting not only its
presence after almost 100 years of its discovery, but also its range of

distribution current in the region. However, due to the few data and
follow-up of this parasitic in Yungas populations, are necessary new
epidemiological studies that include complementary methodology
(molecular techniques, geographical information systems, entomological sampling, among others), and drug administration schemes
to understand this forgotten parasitosis in Northwestern Argentina.

Conict of interest
The authors declare that there is no conict of interest.

Acknowledgements
We want to thank the technicians of Coordinacin Nacional de
Control de Vectores, Ministerio de Salud de la Nacin for their
invaluable help in the collections of the hematic samples. We also
thank laboratory technician N. Garca (Ministerio de Salud de la
Nacin, Delegacin Salta) for her assistance in the conrmation of
parasite identication. This work was partially funded by Ministerio de Salud de la Nacin.

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