Updates on the distribution and host spectrum of Dirofilaria repens in the Republic of Uzbekistan

Abstract

Among the zoonotic mosquito-borne nematodes, Dirofilaria repens and Dirofilaria immitis (Spirurida, Onchocercidae) are highly significant from a public health perspective. While D. immitis is also of major veterinary concern, D. repens is regarded as less pathogenic for carnivores, but is the main causative agent of human dirofilariosis throughout the Old World. In the Republic of Uzbekistan, recent data refer exclusively to D. immitis infection in domestic and wild carnivores, while the current prevalence and distribution of D. repens remain unknown. Between 2015 and 2021, a total of 559 domestic and wild carnivore carcasses were collected and examined by necropsy. All subcutaneous nematodes were collected and identified morphologically. The overall prevalence of D. repens infection was of 11.03% in domestic dogs, Canis familiaris, and 9.29% in wildlife hosts: golden jackals, Canis aureus (11.76%), wolves, Canis lupus (9.09%), red foxes, Vulpes vulpes (9.23%), and jungle cats, Felis chaus (7.14%). Additionally, a human case of subcutaneous D. repens infection was also documented. The present study represents the first recent assessment of the occurrence of the zoonotic filarioid D. repens in the Republic of Uzbekistan. It indicates a wide distribution in domestic dogs and four species of wildlife hosts throughout the country, raising awareness on the public health risks associated with this parasite.

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Vol.:(0123456789)
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Parasitology Research
https://doi.org/10.1007/s00436-021-07347-w
HELMINTHOLOGY - ORIGINAL PAPER
Updates onthedistribution andhost spectrum ofDirofilaria repens
intheRepublic ofUzbekistan
AlisherSafarov1 · FiruzaAkramova2· DjalaliddinAzimov2· AndreiD.Mihalca3· AngelaM.Ionică3
Received: 31 July 2021 / Accepted: 11 October 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
Among the zoonotic mosquito-borne nematodes, Dirofilaria repens and Dirofilaria immitis (Spirurida, Onchocercidae)
are highly significant from a public health perspective. While D. immitis is also of major veterinary concern, D. repens is
regarded as less pathogenic for carnivores, but is the main causative agent of human dirofilariosis throughout the Old World.
In the Republic of Uzbekistan, recent data refer exclusively to D. immitis infection in domestic and wild carnivores, while
the current prevalence and distribution of D. repens remain unknown. Between 2015 and 2021, a total of 559 domestic and
wild carnivore carcasses were collected and examined by necropsy. All subcutaneous nematodes were collected and identified
morphologically. The overall prevalence of D. repens infection was of 11.03% in domestic dogs, Canis familiaris, and 9.29%
in wildlife hosts: golden jackals, Canis aureus (11.76%), wolves, Canis lupus (9.09%), red foxes, Vulpes vulpes (9.23%),
and jungle cats, Felis chaus (7.14%). Additionally, a human case of subcutaneous D. repens infection was also documented.
The present study represents the first recent assessment of the occurrence of the zoonotic filarioid D. repens in the Republic
of Uzbekistan. It indicates a wide distribution in domestic dogs and four species of wildlife hosts throughout the country,
raising awareness on the public health risks associated with this parasite.
Keywords Dirofilaria repens· Distribution· Host· Zoonosis· Uzbekistan
Introduction
Among mosquito-borne zoonotic nematodes, Dirofilaria
repens and Dirofilaria immitis (Spirurida, Onchocerci-
dae) are highly significant from a public health perspective
(Simón etal. 2012). Both species are able to infect a variety
of carnivore species, but the typical host is represented by
the domestic dog, Canis familiaris. The female nematodes
are larviparous, releasing blood-circulating microfilariae,
which can be ingested by numerous species of mosquito
vectors, mainly within the genera Culex, Aedes, and Anoph-
eles (Otranto etal. 2013). While D. immitis is of great veteri-
nary concern due to the severe disease it causes in carnivores
(heartworm disease) and can occasionally infect also humans
(Mendoza-Roldan etal. 2021), D. repens, which resides in
the subcutaneous tissues, is regarded as less pathogenic for
carnivores, but is the main causative agent of human diro-
filariosis throughout the Old World (Capelli etal. 2018).
The Republic of Uzbekistan includes three landscape
zones: plains, foothills, and mountains; having a diverse
vertebrate fauna. Wild and domestic mammals within the
order Carnivora in modern Uzbekistan are represented
by 34 species and subspecies belonging to five families:
Felidae (13 species), Mustelidae (11 species), Canidae (7
species), Ursidae (2 species), and Hyenidae (1 species)
(Shernazarov etal. 2006). Cases of infection with Dirofi-
laria spp. have been previously identified in some of these
animal species. In particular, D. immitis was detected in
domestic dogs Canis lupus familaris and golden jackals,
Canis aureus (Delyanova 1958; Irgashev 1958). During N.
Matchanov’s research on the helminth fauna of dogs in the
Tashkent region, cases of infection of dogs with D. repens
Section Editor: Domenico Otranto
* Alisher Safarov
safarov-alisher@mail.ru
1 State Committee ofVeterinary andLivestock Development
oftheRepublic ofUzbekistan, Tashkent, Uzbekistan
2 Institute ofZoology oftheAcademy ofSciences
oftheRepublic ofUzbekistan, Tashkent, Uzbekistan
3 Department ofParasitology andParasitic Diseases,
University ofAgricultural Sciences andVeterinary Medicine
ofCluj-Napoca, Cluj-Napoca, Romania
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Parasitology Research
1 3
were also identified (Matchanov 1959). D. immitis and D.
repens have also been reported in golden jackals, C. aureus,
and jungle cats, Felis chaus, along the Syrdarya River in
Uzbekistan (Taryannikov 1983). Some human cases pre-
senting with ocular infection have been recorded between
1915 and 1996, presumably caused by D. repens, but with
unclear confirmation (reviewed by Pampiglione and Rivasi
2000). However, the great majority of these reports are out-
dated. Recent data refer exclusively to D. immitis (Azimov
etal. 2019; Norkobilov etal. 2020; Berdibaev 2021), while
the current prevalence and distribution of D. repens remain
unknown. Therefore, the aims of the present study were to
provide updates on the distribution and host spectrum of
D. repens in carnivores from Uzbekistan, and to present a
recent case of human infection.
Materials andmethods
The present study was carried out between 2016 and 2021. A
total of 559 domestic and wild carnivore carcasses were col-
lected and examined at the Laboratory of General Parasitol-
ogy of the Institute of Zoology of the Academy of Sciences
of the Republic of Uzbekistan, by full parasitological nec-
ropsy (Table1). Wild carnivore carcasses were obtained dur-
ing the legal hunting activity or were found dead at various
locations in the Republic of Karakalpakistan (Northwestern
Uzbekistan), Samarkand, and Surkhandarya regions (North-
eastern Uzbekistan). The domestic dogs, screened during
the study, died due to natural causes or were euthanized for
medical reasons, in the city of Tashkent, or rural settings
situated in Northwestern and Northeastern Uzbekistan. The
carcasses were kept frozen at − 20°C until processing. For
each animal, data regarding species, sex, estimated or exact
age in case of wild carnivores and dogs, respectively, and
location of collection were recorded.
All nematodes residing in the subcutaneous tissues were
collected in labeled vials containing 10% formalin. The
collected nematodes were mounted on glass slides and
examined under a light microscope (Microscope mbs-10.
Modern counterpart. msp-2. Lomo). The morphological
identification was carried out according to descriptions and
keys from literature (Anderson and Bain 1976; Kozlov 1977;
Demiaszkiewicz etal. 2011). The statistical analysis was
performed using EpiInfo 7 software (CDC, USA). The prev-
alence and its 95% Confidence Interval (CI) were calculated,
and differences among groups were assessed by chi square
testing and considered significant for p ≤ 0.05.
In the case of one golden jackal necropsied in February
2021, a single nematode was collected in 70% ethanol and
processed by means of molecular tools. The DNA was iso-
lated from a portion weighing approximately 20mg, using a
commercially available kit (ISOLATE II GENOMIC DNA
kit, BioLine, UK), according to the manufacturer’s instruc-
tions. An ~ 670-bp fragment of the cox1 gene of Spirurid
nematodes was amplified by conventional PCR using the
NTF/NTR primer pair, as previously described (Casiraghi
etal. 2001). The PCR product was sequenced using an exter-
nal service (performed at Macrogen Europe, The Nether-
lands) and then compared to other D. repens isolates from
GenBank database by using Basic Local Alignment Tool
(BLAST) analysis.
In 2019, a 32-year-old woman having no travel history,
was admitted to the Syrdarya Regional Oncological Dis-
pensary with complaints of the presence of a tumor in the
left mammary gland. During ultrasound examination, a dis-
placeable formation with a size of 8 × 5mm was revealed
in the left mammary gland, with a preliminary diagnosis of
potential parasitic cyst. The regional lymph nodes were not
enlarged. The formation was excised and found to contain
a slender white nematode, which was collected in formalin
and submitted for identification to The Laboratory of Gen-
eral Parasitology of the Institute of Zoology of the Academy
of Sciences of the Republic of Uzbekistan.
Results
Dirofilaria repens infection indomestic dogs
Out of 290 examined dogs, a total of 32 (11.03%; 95%CI
7.67–15.22) were found to harbor subcutaneous nematodes,
all identified as D repens. The distribution of positive ani-
mals is presented in Table2.
There were no statistically significant differences between
Northeastern and Northwestern Uzbekistan (p = 1). How-
ever, the prevalence in Tashkent megalopolis was signifi-
cantly lower as compared to rural sampling sited from both
Northeastern and Northwestern Uzbekistan (p < 0.0001 in
both cases). The prevalence of infection was significantly
higher in rural sampling areas, in female dogs, and in dogs
aged over 5years (Table3).
Table 1 Carnivore species and number of specimens examined
Family Species Inves-
tigated
specimens
Canidae Domestic dog, Canis familiaris 290
Golden jackal, C. aureus 102
Grey wolf, C. lupus 44
Red fox, Vulpes vulpes 65
Mustelidae Eurasian badger, Meles meles 16
Felidae Jungle cat, Felis chaus 42
Total 559
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The infection rate ranged between 1 and 11 nematodes/
animal.
Dirofilaria repens infection inwild carnivores
Out of the 269 wild carnivores examined, 25 (9.29%; 95%
CI 6.10–13.41) were found to harbor D. repens infection.
Excepting the Eurasian badger, Meles meles, adult D. repens
were found in the subcutaneous tissues of all the examined
wild carnivore species (Table4).
There were no statistically significant differences in the
overall prevalence of infection between regions, neither
globally, nor according to host species (Table5).
The sequence analysis of the D. repens isolate from the
golden jackal revealed a 100% nucleotide identity with five
other D. repens isolates: three from human cases investi-
gated in Europe (KR998257; KX265049; MW017212), one
from a mosquito in Austria (MF695085), and one from a dog
from Lower Austria (MW590257). The sequence was depos-
ited in GenBank under the Accession Number MZ081850.
Human case
The nematode removed from the patient’s breast had a body
length of 52mm, with a maximum width of 3.9mm. The
cuticle presented longitudinal striations on the entire body
length. The anterior extremity was rounded, having a circu-
lar oral opening surrounded by four pairs of cephalic papil-
lae. The posterior extremity was spirally twisted, and two
unequal spicules were visible. Based on these characteris-
tics, it was concluded that the nematode was a male of D.
repens.
Discussion
The occurrence of D. repens was reported on various
occasions in the Republic of Uzbekistan, but no data
from the twenty-first century was available prior to the
present study. Similarly, in neighboring countries, in
Kazakhstan, during the years 1953–1956, infection with
D. repens was found in 42.6% of 970 dogs examined from
the town Kzyl Orda, and in 4.17% of 30,700 Aedes macu-
lipennis sacharovi mosquitoes (Chun-syun 1959). How-
ever, this information is outdated and there is no avail-
able data on research conducted in recent years in Central
Asia. The first molecular survey and confirmation of D.
repens nematode in the Kyrgyz Republic was carried out
recently, in the Bishkek region, with just one dog (0.29%)
being positive (Aydın etal. 2020). In Iran, Tehran prov-
ince, the molecular prevalence of D. repens was 26% in
2017 (Pedram etal. 2019). In Uzbekistan, according to
the centralized data published by Sultanov etal. (1975),
and Muminov (1976), the prevalence of dirofilariosis in
the studied dogs from Uzbekistan showed great varia-
tion, according to environmental conditions: 0.66–2.9%
for D. immitis and 1.4–20% for D. repens. In the present
Table 2 The prevalence of D. repens infection in dogs from Uzbeki-
stan
Region Examined dogs D. repens infection
N % 95% CI
Tashkent 160 5 3.13 1.02–7.14
Northeast 65 13 20.00 11.10–31.77
Northwest 65 14 21.54 12.31–33.49
Total 290 32 11.03 7.67–15.22
Table 3 The distribution of D.
repens infection in domestic
dogs from Uzbekistan
Parameter Examined D. repens p
N % 95% CI
Environment Urban 160 5 3.13 1.02–7.14 < 0.0001
Rural 130 27 20.77 14.16–28.76
Sex M 187 13 6.95 3.75–11.59 0.005
F 103 19 18.45 11.49–27.30
Age ≤ 2 42 0 0 0–8.41 0.0001
2–5 210 21 10.0 6.30–14.88
> 5 38 11 28.95 15.42–45.90
Table 4 The prevalence of D. repens infection in wild carnivores
from Uzbekistan
Species Examined D. repens infection p
n % 95% CI
Canis aureus 102 12 11.76 6.23–19.65 0.624
Canis lupus 44 4 9.09 2.53–21.67
Vulpes vulpes 65 6 9.23 3.46–19.02
Meles meles 16 0 0 0–20.59
Felis chaus 42 3 7.14 1.5–19.48
Total 269 25 9.29 6.10–13.41 -
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Parasitology Research
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study, we report similar values, with the prevalence of D.
repens infection in domestic dogs ranging between 3.13%
and 21.54%. However, the infection rate was significantly
higher in rural dogs as compared to those from an urban
environment. This is probably due to the owner’s increased
awareness and the extensive use of anthelmintics for urban
pet dogs (Panarese etal. 2021). In contrast, in rural areas,
the dogs are often neglected by their owners and are gen-
erally regarded as service animals, therefore they don’t
regularly receive deworming treatments. Although sex is
generally not considered as a risk factor for contracting the
filarial infection (Montoya etal. 2006; Rapti and Rehbein
2010) and in some cases, a higher prevalence is described
in male dogs (Montoya etal. 1998; Scaramozzino etal.
2005; Yildirim etal. 2007), in the present study, the pro-
portion of females infected by D. repens was significantly
higher. The highest prevalence was found in dogs over five
years of age. This is most probably a consequence of a
longer period of exposure to competent vectors, as also in
the case of the heartworm, D. immitis (Rhee etal. 1998).
A recent study performed on domestic dogs from vari-
ous regions of Uzbekistan revealed an overall prevalence
of 9.6% for D. immitis infection, with regional variations
from 5% in urban dogs to 13.2% in rural ones (Norkobilov
etal. 2020). The overall prevalence of D. repens exceeds
that of D. immitis, as also observed in several European
countries (Genchi etal. 2011), and also in Iran (Pedram
etal. 2019). Nevertheless, infected microfilariaemic dogs
serve as the main reservoir of infection, both for other car-
nivores and humans, representing a public health hazard
(Capelli etal. 2018; Brianti etal. 2021).
Previous data indicated the occurrence of D. repens
in two species of wild carnivores in Uzbekistan, namely
the golden jackal, C. aureus, and the jungle cat, F. chaus
(Irgashev 1958; Murtazaev 1964a, b, 1975; Matchanov
1968; Muminov 1968; Sultanov etal. 1969; Taryannikov
1983). Herein, we report two new host-parasite associations
in the country, the gray wolves, C. lupus, and red foxes,
V. vulpes. In the assessed wild carnivores, the prevalence
of D. repens infection did not vary significantly between
host species, indicating a similar susceptibility to infection.
Although infection of wild carnivores is generally regarded
as an epi-phenomenon of dog infection in overlapping ter-
ritories (Otranto etal. 2015), the relatively high prevalence
(9.29%) suggests that wildlife species could also play a role
in the maintenance and dissemination of infection. Fur-
thermore, the involvement of wild carnivores as sources of
human dirofilariosis has never been properly investigated,
but it is estimated that they could play a major epidemio-
logical role, due to the complete lack of preventative control
strategies (Otranto and Deplasez 2020).
The recently documented human case of D. repens infec-
tion was autochthonous, as revealed by the lack of travel
history of the affected patient. The clinical presentation was
subcutaneous, initially regarded as a tumor. This case rep-
resents an alarm, highlighting the necessity of development
Table 5 The distribution
of D. repens infection in
wild carnivore species from
Uzbekistan
Species Region Examined D. repens infection p
N % 95% CI
Canis aureus Karakalpakistan 51 7 13.73 5.70–26.26 0.235
Samarkand 37 2 5.41 0.66–18.19
Surkhandarya 14 3 21.43 4.66–50.80
Canis lupus Karakalpakistan 28 2 7.14 0.88–23.50 0.818
Samarkand 9 1 11.11 0.28–48.25
Surkhandarya 7 1 14.29 0.36–57.87
Vulpes vulpes Karakalpakistan 18 2 11.11 1.38–34.71 0.906
Samarkand 27 2 7.41 0.91–24.29
Surkhandarya 20 2 10.00 1.23–31.70
Meles meles Karakalpakistan 6 0 0 0–45.93 1
Samarkand 3 0 0 0–70.76
Surkhandarya 7 0 0 0–40.96
Felis chaus Karakalpakistan 4 1 25 0.63–80.59 0.254
Samarkand 29 1 3.45 0.09–17.76
Surkhandarya 9 1 11.11 0.28–48.25
Total Karakalpakistan 107 12 11.21 5.93–18.77 0.263
Samarkand 105 6 5.71 2.13–12.02
Surkhandarya 57 7 12.28 5.08–23.68
Northwest 107 12 11.21 5.93–18.77 0.397
Northeast 162 13 8.02 4.34–13.33
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Parasitology Research
1 3
and implementation of solid control strategies, based on
thorough investigation of the infection status of the para-
site’s natural hosts (i.e. domestic dogs) and consequent
mass administration of deworming treatment in the affected
regions. Further studies focused on the identification of
potential vector populations, and implementation of mos-
quito control actions would also be necessary.
Conclusion
The present study represents the first recent assessment of
the occurrence of the zoonotic filarioid D. repens in the
Republic of Uzbekistan and the first molecular confirma-
tion. It indicates a wide distribution in domestic dogs and
four species of wildlife hosts throughout the country, raising
awareness on the public health risks associated with this
parasite.
Acknowledgements We would like to thank the Department of Para-
sitology and Parasitic Diseases, Cluj-Napoca University of Agricul-
tural Sciences and Veterinary Medicine (Romania) for their scientific
cooperation.
Funding This research was carried out on the basis of the research
program of the Institute of Zoology of the Academy of Sciences of
the Republic of Uzbekistan for 2020–2025 on “Improvement of ways
of formation, taxonomy and control measures of vertebrate helminth
fauna” and on the basis of the economic contract “Parasitological moni-
toring of foreign objects (pastries and reservoirs) in Karakalpakistan”
which is planned for implementation in 2021–2022 (No. /4/2021 of
April 13, 2021).
Data availability All relevant data is enclosed within the manuscript.
Code availability Not applicable.
Declarations
Ethics approval and consent to participate Not applicable.
Consent for publication Not applicable.
Conflict of interest The authors declare no competing interests.
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