Abstract
In Uzbekistan, the number of reported leishmaniasis cases is rising at the alarming rate. In this work, we studied the phlebotomine sand fly (Diptera: Phlebotominae) diversity in the foci of cutaneous leishmaniasis in the Surxondaryo Region of Uzbekistan and compared it with the data obtained for the same area 50 years ago, when infection prevalence was reportedly low. We found that the implicated vector for zoonotic leishmaniasis, P. papatasi, remained eudominant; the proportion of implicated anthroponotic leishmaniasis vector, P. sergenti, rose significantly from averaged 5.4 to 41.4%; Phlebotomus alexandri, a suspected visceral leishmaniasis vector, was eudominant at two sites, and a second suspected vector for this disease, P. longiductus, was newly recorded in the region. We conclude that the increase in the documented cases of cutaneous leishmaniasis in the Surxondaryo Region of Uzbekistan may be connected to the changes in fauna of sand flies vectoring Leishmania spp.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
In Uzbekistan, leishmaniasis—a neglected vector-borne disease caused by Leishmania spp. (Kinetoplastea: Trypanosomatidae) (Bruschi and Gradoni 2018; Kostygov et al. 2024)—is a serious problem and the number of cases is on the rise (Mustanov and Nematov 2019; Strelkova et al. 2015; Suvonkulov et al. 2020; Yurchenko et al. 2023). These parasites are dispersed worldwide and affect up to 15 million people in about 100 (mainly, tropical and subtropical) countries (WHO 2023). By clinical manifestation, leishmaniasis can be cutaneous (CL) and visceral (VL) resulting in often self-healing skin ulcers and multiorgan damage, respectively (Burza et al. 2018; Mann et al. 2021). Both forms are present in Uzbekistan (Alam et al. 2009; Mustafaev 1991; Shishliaeva-Matova et al. 1966; Strelkova et al. 2015; Zhirenkina et al. 2011). These diseases are caused by different and usually not overlapping sets of Leishmania spp. in the region: L. infantum complex for VL and L. major and L. tropica for CL serving as the etiologic agents for zoonotic (ZCL) and anthroponotic (ACL) leishmaniasis, respectively (Akilov et al. 2007; Bruschi and Gradoni 2018; Ghatee et al. 2020; Yurchenko et al. 2023).
The geographical focus of this work is Surxondaryo (Surkhandarya) Region of Uzbekistan. This choice was determined by the following factors: (1) the highest prevalence and alarmingly positive dynamics of leishmaniasis here compared to other regions (Suvonkulov et al. 2020) and (2) the availability of historical studies for comparative analysis with a drawback of many papers published in Russian and never translated into English (Kogay 1960; Latyshev and Krukova 1941; Lugina 1959). As a matter of fact, the seminal discovery that two different subspecies (now, species) of Leishmania—L. tropica minor (now, L. tropica) and L. tropica major (now, L. major)—cause ACL and ZCL was done in Termez (now, Termiz; low Surxondaryo Region) by Yakimov and Schokhor, 1914 (Yakimov and Schokhor 1914). The systematic records of disease prevalence in this recognized focus of ZCL date back to 1932 (Dukelski and Rait 1932; Latyshev and Krukova 1941; Nasyrov and Yusupov 1974). Before the implementation of the mandatory prophylactic measures in the USSR in 1960–1970s (Kellina and Morozov 1982; Sergiev et al. 2018), the ZCL in Surxondaryo Region was not as widespread as in other regions of the country and restricted to just six reported localities (Ipatov and Zviagintseva 1967; Isaev 1959). It should be noted though that this number is most likely a severe underestimate due to the lack of reporting in many areas. The disease was practically eradicated by the mid-1980s (Sergiev et al. 2018; Sharipov et al. 1986), yet, following the collapse of the Soviet Union, it has returned “with vengeance” (Mustanov and Nematov 2019; Suvonkulov et al. 2020).
One of the potential reasons for such a comeback is the population dynamics of Leishmania spp. vectors. Indeed, complex measures targeting both the vectors and animal reservoirs applied in the second half of the last century led to a sharp drop in leishmaniasis prevalence (Sharipov et al. 1986). In this work, we investigated the phlebotomine sand fly (Diptera: Phlebotominae) diversity in the foci of cutaneous leishmaniasis in the Surxondaryo Region of Uzbekistan and compared it with the data obtained for the same area 50 years ago, when infection prevalence was reportedly low. We believe that these data will be valuable for developing effective control measures for sand fly in their natural habitats.
Methods
The Surxondaryo is southernmost Region of Uzbekistan (Fig. 1). It features diverse landscapes from the plains of the Amu Darya river valley in the central and southern parts to the mountain ranges in the northern, eastern, and western parts. The climate here is warm with temperatures reaching + 45–60 °C in July; winters are short. In the plains and mountain foothill areas, the precipitation ranges from 130–360 mm to 440–620 mm annually, respectively.
Sand flies were collected in the summer months (June–August) of 2021 and 2022 in six stationary points in the Surxondaryo Region (Altynsay [38.2390° N, 67.6055° E, Altynsay District]—1 household; Boysun [38.1977° N, 67.2014° E, Boysun District]—1 household; Dekhanabad [37.6785° N, 67.0536° E, Sherabod District]—2 households; Poshxurd [37.7002° N, 66.7770° E, Sherobod District]—2 households; Sina [38.3603° N, 67.6841° E, Denov District]—3 households; Termiz [37.2611° N, 67.3086° E, Termiz District]—2 households), where leishmaniasis cases were registered (Fig. 1). The households, in which sand flies were caught, are traditional for Uzbekistan and consist of a residential building, sheds for keeping large and small livestock, a poultry house, a shed for firewood storage, and an outdoor toilet. There are usually several fruit trees and a vegetable/ornamental garden in the yard. Pets (typically, cats and dogs) are kept outside. The abundance of organic matter in the places protected from the direct sunlight and high humidity creates optimal conditions for the development of sand flies. Sand fly collection, fixation in gum arabic, and species identification were performed as described previously (Artemiev and Neronov 1984; Zvancov 2019). In short, sticky traps (approximately, 300 in total) were placed at a height of 50 to 150 cm in the evening and collected the following morning. Trapped sand flies were fixed in ethanol first before permanent fixation in the Fora-Berleze gum Arabic medium. Potential sand fly breeding sites (premises for keeping animals, sheds (including those used for dung storage), toilets, and residential areas) were examined separately. Historical data from 1966 to 1971 (Dzhabarov 1972; Zviagintseva 1968) (based on the analysis of 13,500 sand fly specimens in total) are shown in Table 1.
Results and discussion
Analysis of sand fly diversity in the Surxondaryo Region of Uzbekistan in 2021–2022
A total of 969 sand flies of the two genera Phlebotomus (4 spp.) and Sergentomyia (2 spp.) were collected and analyzed (Table 1). Expectedly, two Phlebotomus sp.: P. (Phlebotomus) papatasi and P. (Paraphlebotomus) sergenti constitute the vast majority (over 80%) of the collected material since it was focused on the households with reported cases of leishmaniasis. This is a good representation of the 11 species of sand flies (P. (Paraphlebotomus) alexandri, P. (Paraphlebotomus) andrejevi, P. (Paraphlebotomus) cauacasicus, P. (Paraphlebotomus) mongolensis, P. (Phlebotomus) papatasi, P. (Paraphlebotomus) sergenti, P. (Larroussius) smirnovi, S. (Sergentomyia) arpaklensis, S. (Sintonius) clydei, S. grecovi, and S. sogdiana) previously documented in the Uzbek CL foci (Shishliaeva-Matova et al. 1966; Zviagintseva 1968). Five species not detected in our dataset always represented minor fractions in the collections analyzed earlier. The basic criteria for defining the vector include proof that the geographical distributions of the vector and the human disease overlap, that the sand fly species is anthropophilic, and that the same Leishmania sp. has been repeatedly isolated and identified in sand flies and patients. Supporting observations should demonstrate that the specific sand fly commonly feeds on reservoir hosts and can support both the development and transmission of the parasite (Killick-Kendrick 1990; Ready 2013). Sand flies can display a strong preference for a given Leishmania sp. (specific vectors) or allow the development of several Leishmania spp. (permissive vectors) (Alexandre et al. 2020; Dobson et al. 2010; Dostálová and Volf 2012; Dvorák et al. 2018; Kamhawi et al. 2000; Volf and Myšková 2007). Proven vectors of L. major and L. tropica in Central Asia are P. papatasi and P. sergenti, respectively (Maroli et al. 2013). In addition, three species of the P. caucasicus complex (P. caucasicus, P. mongolensis, and P. andrejevi) were shown to transmit L. major to animal hosts, but their involvement in the transmission to humans has not been demonstrated (Dvorák et al. 2018; Strelkova 1996), although P. caucasicus and P. (Ph.) salehi are considered proven vectors of L. major in Iran (Maroli et al. 2013). The proven vectors of L. infantum among the Asian species are P. alexandri, P. (Adlerius) chinensis, P. (Ad.) sichuanensis, P. (La.) smirnovi, and P. (La.) wui in China; P. (Ad.) longiductus in Kazakhstan; P. (La.) major s.l. and P. (La.) transcaucasicus in Iran; and P. (Ad.) turanicus in Turkmenistan (Maroli et al. 2013). Phlebotomus (Ad.) longiductus is the vector of L. infantum in Kazakhstan and western China (Dergacheva and Strelkova 1985; Guan et al. 2016) and L. donovani in Himalayan regions of India (Sharma and Singh 2008). This species is also considered the most likely vector transmitting VL in the Surxondaryo Region (Dergacheva and Strelkova 1985; Maroli et al. 2001). Of note, the competence of Leishmania spp. vectors is not fixed and may vary in different ecological and epidemiological settings (Ready 2013).
Most of the collected sand flies were males (ranging from 61% for P. papatasi to over 90% for S. grecovi) (Suppl. Table 1). This confirms previous report from this and other areas on difference in mobility of sand fly sexes (Boussaa et al. 2016; Maroli et al. 2001; Yared et al. 2017). Sand fly distribution in different parts of the household (Suppl. Table 1) is also unremarkable. Except for P. longiductus (absent in living areas) and S. sogdiana (caught only in sheds and yards), all other species were most abundant in the sheds. However, the low number of collected specimens precluded us from making solid conclusions in this regard.
It should be noted that most of the previous studies were focused on southern (low) Surxondaryo Region (Dzhabarov 1972; Ipatov and Zviagintseva 1967; Isaev 1959; Zviagintseva 1968). The presented study extended the analyzed area northward. This is where (Boysun and Sina) a likely vector for VL-causing L. infantum, P. longiductus, was found. Notably, its prevalence is comparable to that documented in the VL foci of Pap district (Fergana Valley) of Namangan Region, Uzbekistan (Maroli et al. 2001). In addition, the fraction of P. sergenti (associated with L. tropica and ACL) in Boysun was shown to be extremely high (over 87%) indicating an active focus of ACL in this locality.
Analysis of sand fly diversity in the Surxondaryo Region of Uzbekistan: comparative study
In this study, our primary question focused on whether the increase in leishmaniasis cases in the Surxondaryo Region is linked to the population dynamics of Leishmania vectors. In comparison with 1966–1971 studies (Dzhabarov 1972; Zviagintseva 1968), we noted the following: (i) the implicated ZCL vector, P. papatasi, remained eudominant (with a sole exception of Boysun), where it was shown to be subdominant, but this locality has not been studied previously; (ii) the proportion of implicated ACL vector, P. sergenti (now, eudominant in all the sampled locations), rose significantly from averaged 5.4% (Dzhabarov 1972) to 41.4%; (iii) neither P. andrejevi nor P. caucasicus, P. mongolensis, or S. arpaklensis were detected in 2021–2022; (iv) the proportion of two Sergentomyia spp., S. grecovi and S. sogdiana, implicated in transmission of reptile parasites of the subgenus Leishmania (Sauroleishmania) (Maroli et al. 1988; Ovezmukhammedov and Saf’janova 1989; Tichá et al. 2023) became more prominent while S. arpaklensis has not been found even in Termiz, where it was previously eudominant; (v) Phlebotomus alexandri, a suspected VL vector, was eudominant at two sites and a second suspected vector for the VL-causing L. infantum, P. longiductus, was newly recorded in the region.
We conclude that the increase in the documented cases of leishmaniasis in the Surxondaryo Region of Uzbekistan may be connected to the changes in the fauna of sand flies vectoring Leishmania spp. although the reasons underlying this must be investigated further. It implies that more drastic measures of control and detection (in humans, animal reservoirs, and vectors) should be implemented to slow down or stop this alarming trend. The fight against leishmaniasis is a complicated challenge. There are still no vaccines available and the transmission of the disease is a complex chain of many elements. From an epidemiological and public health point of view, it is important to establish new prevention and control programs. People should use mosquito nets to protect dwellings and repellents for outdoor activities at dusk when vector activity is high.
Data availability
The data supporting the findings of this study are available within the article and its supplementary materials.
References
Akilov OE, Khachemoune A, Hasan T (2007) Clinical manifestations and classification of Old World cutaneous leishmaniasis. Int J Dermatol 46(2):132–142
Alam MZ et al (2009) Identification of the agent causing visceral leishmaniasis in Uzbeki and Tajiki foci by analysing parasite DNA extracted from patients’ Giemsa-stained tissue preparations. Parasitology 136(9):981–986
Alexandre J et al (2020) Experimental infections and co-infections with Leishmania braziliensis and Leishmania infantum in two sand fly species, Lutzomyia migonei and Lutzomyia longipalpis. Sci Rep 10(1):3566
Artemiev MM, Neronov VM (1984) Distribution and ecology of sandflies of the Old World (genus Phlebotomus). Institute of Evolutionary Morphology and Animal Ecology USSR Academy of Sciences, Moscow (in Russian)
Boussaa S, Kahime K, Samy AM, Salem AB, Boumezzough A (2016) Species composition of sand flies and bionomics of Phlebotomus papatasi and P. sergenti (Diptera: Psychodidae) in cutaneous leishmaniasis endemic foci. Morocco Parasit Vectors 9:60
Bruschi F, Gradoni L (2018) The leishmaniases: old neglected tropical diseases. Springer, Cham, Switzerland
Burza S, Croft SL, Boelaert M (2018) Leishmaniasis Lancet 392(10151):951–970
Dergacheva TI, Strelkova MV (1985) Epidemiological role of sandflies Phlebotomus smirnovi Perfiliev, 1941 and P. longiductus 1928 in visceral leishmaniasis foci in the Kazakh SSR. Trans R Soc Trop Med Hyg 79(1):34–36
Dobson DE, Kamhawi S, Lawyer P, Turco SJ, Beverley SM, Sacks DL (2010) Leishmania major survival in selective Phlebotomus papatasi sand fly vector requires a specific SCG-encoded lipophosphoglycan galactosylation pattern. PLoS Pathog 6(11):e1001185
Dostálová A, Volf P (2012) Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors 5:276
Dukelski B, Rait T (1932) Oriental ulcer and its treatment with X-rays. Vestn Rentgenol Radiol XI:1–4 (in Russian)
Dvorák V, Shaw JJ, Volf P (2018) Parasite biology: the vectors. In: Bruschi F, Gradoni L (eds) The leishmaniases: old neglected tropical diseases. Springer, Cham, Switzerland, pp 31–77
Dzhabarov LN (1972) Cutaneous leishmanisis of the rural type in Surkhandarya Region and measures of its prophylaxis Ministry of Health, Uzbek SSR. (in Russian)
Ghatee MA, Taylor WR, Karamian M (2020) The geographical distribution of cutaneous leishmaniasis causative agents in Iran and its neighboring countries, a review. Front Public Health 8:11
Guan LR, Zhou ZB, Jin CF, Fu Q, Chai JJ (2016) Phlebotomine sand flies (Diptera: Psychodidae) transmitting visceral leishmaniasis and their geographical distribution in China: a review. Infect Dis Poverty 5:15
Ipatov VI, Zviagintseva TV (1967) On spontaneous infection of Severtzov’s jerboa (Allagtaga severtzovi vinogradov) with Leishmania tropica v major. Parazitologiia 1(3):263–264 (in Russian)
Isaev LM (1959) Eradication of leishmaniasis in the USSR during the 7-year-plan. Med Parazitol (Mosk) 28(3):323–327 (in Russian)
Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL (2000) The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121:25–33
Kellina OI, Morozov VI (1982) Epidemiological assessment of the data on the incidence of leishmaniasis in the USSR. Med Parazitol (Mosk) 51(6):49–52 (in Russian)
Killick-Kendrick R (1990) Phlebotomine vectors of the leishmaniases: a review. Med Vet Entomol 4(1):1–24
Kogay ES (1960) On the issue of vectors of cutaneous leishmaniasis and the spread of this disease in the areas of the Surkhandarya region. Uzbek Biol J 4:53–54 (in Russian)
Kostygov AY, Albanaz ATS, Butenko A, Gerasimov ES, Lukeš J, Yurchenko V (2024) Phylogenetic framework to explore trait evolution in Trypanosomatidae. Trends Parasitol 40(2):96–99
Latyshev NI, Krukova AP (1941) On the epidemiology of the cutaneous leishmaniasis. The cutaneous leishmaniasis as zoonotic disease of wild rodents in Turkmenia Proceedings of the Military Medical Academy of the Red Army. vol 25, Leningrad, p 229–242 (in Russian)
Lugina VA (1959) Prevention of cutaneous leishmaniasis in natural foci. Voen Med Zh No 8:39–42 (in Russian)
Mann S et al (2021) A review of leishmaniasis: current knowledge and future directions. Curr Trop Med Rep 8(2):121–132
Maroli M, Gramiccia M, Gradoni L, Ready PD, Smith DF, Aquino C (1988) Natural infections of phlebotomine sandflies with Trypanosomatidae in central and south Italy. Trans R Soc Trop Med Hyg 82(2):227–228
Maroli M, Krasnonos L, Gafurov I (2001) Epidemiological and entomological survey in a focus of visceral leishmaniasis in Pap district (Fergana Valley) of Namangan region, Uzbekistan Acta Trop 80(3):223–228
Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L (2013) Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol 27(2):123–147
Mustafaev KM (1991) The epidemiological situation regarding zoonotic cutaneous leishmaniasis in Uzbekistan. Med Parazitol (Mosk) 1991(6):15–17 (in Russian)
Mustanov ZA, Nematov AS (2019) Retrospective epidemiological analysis of the leishmaniasis in Uzbekistan. Bacteriology 4(4):47–49
Nasyrov FS, Yusupov KA (1974) Virulence and pathogenicity factors of Leishmania strains from the Lower Surkhan Darya focus of cutaneous leishmaniasis. Parazitologiia 8(1):77–81 (in Russian)
Ovezmukhammedov A, Saf’janova VM (1989) Taxonomic problems of the Leishmania of reptiles. Parazitologiia 23(4):334–343 (in Russian)
Ready PD (2013) Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 58:227–250
Sergiev V et al (2018) Epidemiology and control of leishmaniasis in the former USSR: a review article. Iran J Parasitol 13(3):342–350
Sharipov MK, Razakov ShA, Krasnonos LN, Iusupov KA, Mansurov AA (1986) Zoonotic cutaneous leishmaniasis in the Uzbek SSR and its prevention. Med Parazitol (Mosk) 1:39–45 (in Russian)
Sharma U, Singh S (2008) Insect vectors of Leishmania: distribution, physiology and their control. J Vector Borne Dis 45(4):255–272
Shishliaeva-Matova ZS, Ni G, Zviagintseva TV (1966) Pathogenicity of leptomonad strains isolated from sandflies in natural foci of zoonotic cutaneous leishmaniasis in Uzbekistan. Med Parazitol (Mosk) 35(3):266–270 (in Russian)
Strelkova MV (1996) Progress in studies on Central Asian foci of zoonotic cutaneous leishmaniasis: a review. Folia Parasitol 43(1):1–6
Strelkova MV et al (2015) A narrative review of visceral leishmaniasis in Armenia, Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan, the Crimean Peninsula and Southern Russia. Parasit Vectors 8:330
Suvonkulov UT et al (2020) Prevalence of cutaneous leishmaniasis among population in endemic regions of Uzbekistan. Soc Innovat SI1:592–597
Tichá L et al (2023) Experimental feeding of Sergentomyia minuta on reptiles and mammals: comparison with Phlebotomus papatasi. Parasit Vectors 16(1):126
Volf P, Myšková J (2007) Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol 23(3):91–92
WHO (2023) Leishmaniasis. https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis. Accessed 15 Jan 2024
Yakimov WL, Schokhor NI (1914) Réserches sur les maladies tropicales humaines et animales au Turkestan – II. La leishmaniose cutanée spontanée du chien au Turkestan. Bull Soc Pathol Exot 7:186–187
Yared S et al (2017) Diversity and altitudinal distribution of phlebotomine sand flies (Diptera: Psychodidae) in visceral leishmaniasis endemic areas of northwest Ethiopia. Acta Trop 176:1–10
Yurchenko V, Chistyakov DS, Akhmadishina LV, Lukashev AN, Sádlová J, Strelkova MV (2023) Revisiting epidemiology of leishmaniasis in Central Asia: lessons learnt. Parasitology 150(2):129–136
Zhirenkina EN et al (2011) The epidemiological features of visceral leishmaniasis, revealed on examination of children by Polymerase Chain Reaction, in the Papsky District, Namangan Region, Uzbekistan. Med Parazitol (Mosk)(3):37–41 (in Russian)
Zvancov AB (2019) Identifier of sandflies (Diptera, Psychodidae, Phlebotominae) of Central Asia. WHO Regional Office for Europe. (in Russian)
Zviagintseva TV (1968) Aggressiveness of different species of sandflies towards man and their infection rate with L. tropica major at the moment of blood-sucking. Med Parazitol (Mosk) 37(5):570–574 (in Russian)
Funding
Open access publishing supported by the National Technical Library in Prague. This work was supported by the European Union’s LERCO Operational Program “Just Transition” (CZ.10.03.01/00/22_003/0000003) to V.Y.
Author information
Authors and Affiliations
Contributions
Study design: G.X.U. and V.S.T. Data collection: G.X.U. and V.S.T. Data analysis: G.X.U., X.G.S., J.S., J.A.M., A.S., V.Y. Manuscript preparation (draft): G.X.U. and V.Y. All authors contributed to the final draft and editing, giving their approval for publication and agreeing to be held accountable for the work performed herein.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Handling Editor: Una Ryan
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
436_2024_8191_MOESM1_ESM.docx
Supplementary file1 Suppl Table 1. Sand flies’ habitats. The numbers of caught sandflies are shown for 1 – living area; 2 – shed; 3 – poultry house; 4 – firewood storage; 5 – yard; 6 – toilet. The proportion of collected male sand flies is shown in parentheses in the second column. (DOCX 22 KB)
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Usarov, G.X., Turitsin, V.S., Sattarova, X.G. et al. Phlebotomine sand fly (Diptera: Phlebotominae) diversity in the foci of cutaneous leishmaniasis in the Surxondaryo Region of Uzbekistan: 50 years on. Parasitol Res 123, 170 (2024). https://doi.org/10.1007/s00436-024-08191-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00436-024-08191-4