Angiostrongylus minasensis n. sp.: nova espécie encontrada parasitando quatis (Nasua nasua) em área de proteção urbana no Brasil

Almeida, Lara Ribeiro de; Souza, Joyce Gonçalves Rosário de; Santos, Hudson Andrade; Torres, Eduardo José Lopes; Vilela, Roberto do Val; Cruz, Olívia Monique Soares; Rodrigues, Leonardo; Pereira, Cíntia Aparecida de Jesus; Maldonado Junior, Arnaldo; Lima, Walter dos Santos

Lara Ribeiro de Almeida

Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, MG, Brasil

Joyce Gonçalves Rosário de Souza

Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz – FIOCRUZ, Rio de Janeiro, RJ, Brasil

Hudson Andrade Santos

Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, MG, Brasil

Eduardo José Lopes Torres

Laboratório de Helmintologia Romero Lascasas Porto, Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Centro Biomédico, Universidade do Estado do Rio de Janeiro – UERJ, Rio de Janeiro, RJ, Brasil

Roberto do Val Vilela

Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz – FIOCRUZ, Rio de Janeiro, RJ, Brasil

Olívia Monique Soares Cruz

Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, MG, Brasil

Leonardo Rodrigues

Escola Estadual de Ensino Fundamental e Médio Graça Aranha, Secretaria da Educação – SEDU, Santa Maria de Jetibá, ES, Brasil

Cíntia Aparecida de Jesus Pereira

Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, MG, Brasil

Arnaldo Maldonado Junior

Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Fundação Oswaldo Cruz – FIOCRUZ, Rio de Janeiro, RJ, Brasil

Walter dos Santos Lima ^**Corresponding author: Walter dos Santos Lima. E-mail: wlima@icb.ufmg.br

Laboratório de Helmintologia Veterinária, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Belo Horizonte, MG, Brasil

https://orcid.org/0000-0002-1059-3589

*Corresponding author: Walter dos Santos Lima. E-mail: wlima@icb.ufmg.br

Referred species	GenBank accession	Host	Site of infection	Geographical origin	Reference
Necator americanus	AJ417719	Human	Small intestine	China	Hu et al. (2002)Hu M, Chilton NB, Gasser RB. The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: secernentea). Int J Parasitol 2002; 32(2): 145-158. http://dx.doi.org/10.1016/S0020-7519(01)00316-2. PMid:11812491. http://dx.doi.org/10.1016/S0020-7519(01)...
Ancylostoma duodenale	AJ417718	Human	Small intestine	China	Hu et al. (2002)Hu M, Chilton NB, Gasser RB. The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: secernentea). Int J Parasitol 2002; 32(2): 145-158. http://dx.doi.org/10.1016/S0020-7519(01)00316-2. PMid:11812491. http://dx.doi.org/10.1016/S0020-7519(01)...
Aelurostrongylus abstrusus	JX519458	Felis catus	Lung	-	Jabbar et al. (2013a)Jabbar A, Jex AR, Mohandas N, Hall RS, Littlewood DTJ, Gasser RB. The mitochondrial genome of Aelurostrongylus abstrusus diagnostic, epidemiological and systematic implications. Gene 2013a; 516(2): 294-300. http://dx.doi.org/10.1016/j.gene.2012.10.072. PMid:23142387. http://dx.doi.org/10.1016/j.gene.2012.10...
Heterostrongylus heterostrongylus	XXXXX	Didelphis aurita	Lung	Brazil	Costa et al. (2016)Costa SF No, Oliveira Simões R, Mota ÉM, Val Vilela R, Lopes Torres EJ, Santos Barbosa H, et al. Lungworm Heterostrongylus heterostrongylus Travassos, 1925 from the black-eared opossum in South America: Morphologic, histopathological and phylogenetic aspects. Vet Parasitol 2016; 228: 144-152. http://dx.doi.org/10.1016/j.vetpar.2016.08.018. PMid:27692317. http://dx.doi.org/10.1016/j.vetpar.2016....
H. heterostrongylus	XXXXX	Didelphis aurita	Lung	Brazil	Costa et al. (2016)Costa SF No, Oliveira Simões R, Mota ÉM, Val Vilela R, Lopes Torres EJ, Santos Barbosa H, et al. Lungworm Heterostrongylus heterostrongylus Travassos, 1925 from the black-eared opossum in South America: Morphologic, histopathological and phylogenetic aspects. Vet Parasitol 2016; 228: 144-152. http://dx.doi.org/10.1016/j.vetpar.2016.08.018. PMid:27692317. http://dx.doi.org/10.1016/j.vetpar.2016....
Metastrongylus pudendotectus	NC_013813	Pig	Terminal bronchi in the lungs	Estonia	Jex et al. (2010)Jex AR, Hall RS, Littlewood DTJ, Gasser RB. An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Res 2010; 38(2): 522-533. http://dx.doi.org/10.1093/nar/gkp883. PMid:19892826. http://dx.doi.org/10.1093/nar/gkp883...
Metastrongylus salmi	NC_013815	Pig	Terminal bronchi in the lungs	Estonia	Jex et al. (2010)Jex AR, Hall RS, Littlewood DTJ, Gasser RB. An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Res 2010; 38(2): 522-533. http://dx.doi.org/10.1093/nar/gkp883. PMid:19892826. http://dx.doi.org/10.1093/nar/gkp883...
Parafilaroides normani	NC_024656	Arctocephalus pusillus	Lung	Australia	Jabbar et al. (2014)Jabbar A, Mohandas N, Gasser RB. Characterisation of the mitochondrial genome of Parafilaroides normani (lungworm) of Arctocephalus pusillus doriferus (Australian fur seal). Parasitol Res 2014; 113(8): 3049-3055. http://dx.doi.org/10.1007/s00436-014-3968-8. PMid:24924434. http://dx.doi.org/10.1007/s00436-014-396...
Protostrongylus rufescens	NC_023262	Sheep	Lung	Australia	Jabbar et al. (2013b)Jabbar A, Mohandas N, Jex AR, Gasser RB. The mitochondrial genome of Protostrongylus rufescens– implications for population and systematic studies. Parasit Vectors 2013b; 6(1): 263. http://dx.doi.org/10.1186/1756-3305-6-263. PMid:24025317. http://dx.doi.org/10.1186/1756-3305-6-26...
Angiostrongylus vasorum	GQ982735	Canis familiaris	Heart and pulmonary arteries	United Kingdom	Jefferies et al. (2010)Jefferies R, Shaw SE, Willesen J, Viney ME, Morgan ER. Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infect Genet Evol 2010; 10(4): 561-568. http://dx.doi.org/10.1016/j.meegid.2010.01.013. PMid:20139034. http://dx.doi.org/10.1016/j.meegid.2010....
A. vasorum	GQ982871	Vulpes vulpes	Heart and pulmonary arteries	Portugal	Jefferies et al. (2010)Jefferies R, Shaw SE, Willesen J, Viney ME, Morgan ER. Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infect Genet Evol 2010; 10(4): 561-568. http://dx.doi.org/10.1016/j.meegid.2010.01.013. PMid:20139034. http://dx.doi.org/10.1016/j.meegid.2010....
A. chabaudi	KU521521	Felis silvestris	Heart and pulmonary arteries	Romania	Gherman et al. (2016)Gherman CM, Ionică AM, D’Amico G, Otranto D, Mihalca AD. Angiostrongylus chabaudi (Biocca, 1957) in wildcat (Felis silvestris silvestris, S) from Romania. Parasitol Res 2016; 115(6): 2511-2517. http://dx.doi.org/10.1007/s00436-016-5032-3. PMid:27106235. http://dx.doi.org/10.1007/s00436-016-503...
A. cantonensis	GQ398121	Rattus norvegicus	Pulmonary arteries	China	Lv et al. (2012)Lv S, Zhang Y, Zhang L, Liu Q, Liu HX, Hu L, et al. The complete mitochondrial genome of the rodent intra-arterial nematodes Angiostrongylus cantonensis and Angiostrongylus costaricensis. Parasitol Res 2012; 111(1): 115-123. http://dx.doi.org/10.1007/s00436-011-2807-4. PMid:22246368. http://dx.doi.org/10.1007/s00436-011-280...
A. malaysiensis	KT947979	Rattus rattus	Heart and lung	Malaysia	Yong et al. (2016)Yong HS, Song SL, Eamsobhana P, Lim PE. Complete mitochondrial genome of Angiostrongylus malaysiensis lungworm and molecular phylogeny of Metastrongyloid nematodes. Acta Trop 2016; 161: 33-40. http://dx.doi.org/10.1016/j.actatropica.2016.05.002. PMid:27207134. http://dx.doi.org/10.1016/j.actatropica....
A. costaricensis	KX378965	Nasua narica	Mesenteric vessels	Costa Rica	Santoro et al. (2016)Santoro M, Alfaro-Alarcón A, Veneziano V, Cerrone A, Latrofa MS, Otranto D, et al. The white-nosed coati (Nasua narica) is a naturally susceptible definitive host for the zoonotic nematode Angiostrongylus costaricensis in Costa Rica. Vet Parasitol 2016; 228: 93-95. http://dx.doi.org/10.1016/j.vetpar.2016.08.017. PMid:27692339. http://dx.doi.org/10.1016/j.vetpar.2016....
A. costaricensis	KR827449	-	Mesenteric vessels	Costa Rica	Yong et al., (2015)Yong HS, Song SL, Eamsobhana P, Goh SY, Lim PE, Chow WL, et al. Mitochondrial genome supports sibling species of Angiostrongylus costaricensis (Nematoda: angiostrongylidae). PLoS One 2015; 10(7): e0134581. http://dx.doi.org/10.1371/journal.pone.0134581. PMid:26230642. http://dx.doi.org/10.1371/journal.pone.0...
A. costaricensis	GQ398122	-	Mesenteric vessels	Brazil	Lv et al. (2012)Lv S, Zhang Y, Zhang L, Liu Q, Liu HX, Hu L, et al. The complete mitochondrial genome of the rodent intra-arterial nematodes Angiostrongylus cantonensis and Angiostrongylus costaricensis. Parasitol Res 2012; 111(1): 115-123. http://dx.doi.org/10.1007/s00436-011-2807-4. PMid:22246368. http://dx.doi.org/10.1007/s00436-011-280...
A. minasensis n. sp.	XXXXX	Nasua nasua	Mesenteric vessels	Brazil	Present study

	*A. minasensis*	*A. costaricensis*	*A. siamensis*	*A. gubernaculatus*	*A. vasorum*	*A. chabaudi*
Reference		Morera & Céspedes (1970)Morera P, Céspedes R. Angiostrongylus costaricensis n. sp. (Nematoda: Metastrongyloidea), a new lungworm occurring in man in Costa Rica. Rev Biol Trop 1970; 18(1): 173-185. PMid:5527668.	Ohbayashi et al. (1979)Ohbayashi M, Kamiya M, Bhaibulaya M. Studies on the parasite fauna of Thailand I. Two new metastrongylid nematodes, Angiostrongylus siamensis sp. n. and Thaistrongylus harinasutai gen. et sp. n. (Metastrongyloidea; Angiostrongylidae) from wild rats. Jpn J Vet Res 1979; 27(1-2): 5-10. PMid:529658.	Dougherty (1946)Dougherty EC. The genus Aelurostrongylus Cameron, 1927 (Nematoda: Metastrongylidae) and its relatives; with descriptions of Parafilaroides gen. nov., and Angiostrongylus gubernaculatus sp. nov. Proc Helminthol Soc Wash 1946; 13: 16-26. PMid:21026155.	Guilhon & Cens (1973)Guilhon J, Cens B. Angiostrongylus vasorum (Baillet, 1866): étude biologique et morphologique. Ann Parasitol Hum Comp 1973; 48(4): 567-596. http://dx.doi.org/10.1051/parasite/1973484567. PMid:4791829. http://dx.doi.org/10.1051/parasite/19734...	Biocca (1957)Biocca E. Angiostrongylus chabaudi n. sp. parassita del cuore e dei vasi polmonari del gatto selvatico (Felis silvestris). Lincei Rend Sc Fis Mat Nat. 1957; 22(4): 526-532.
Host	Nasua nasua	Man	Rattus sabanus, R. berdmorei	Taxidea taxus neglecta Mearns	Canis lupus familiaris	Felis silvestris
Locality	Brazil	Costa Rica	Thailand	California	France	Central Italy
MALE
Length	12.12-14.1	15.0-17.9	10	18-19.5	14-15.5	14.6-16.3
Width	0.19-0.22	-	-	0.3	-	0.185-0.225
Oesophagus	0.2-0.25	0.16-0.18	0.23	0.3-0.34	0.22-0.28	0.3-0.345
Nerve ring	0.064-0.075	-	-	-	0.08-0.092	0.185-0.23
Excretory pore	0.3-0.37	-	0.32	-	0.31-0.35	0.335-0.405
Spicule	0.24-0.27	0.267-0.297	0.339	0.52-0.56	0.4-0.48	0.510-0.555
Gubernaculum	0.034-0.045	Present	Present	0.045-0.05	0-04-0.055	Absent
FEMALE
Length	16.25-20.83	26.9	11-13	22-24	15-20.5	19.8-24.1
Width	0.23-0.26	-	-	0.35	-	0.245-0.298
Oesophagus	0.22-0.26	0.10-0.26	0.23-0.27	0.34-0.35	0.24-0.28	0.345-0.38
Nerve ring	0.066- 0.073	-	-	-	0.08-0.096	0.21-0.24
Excretory pore	0.38-0.44	-	0.32-0.36	-	0.35-0.37	0.395-0.47
Vulva-tail	0.31-0.37	0.175	0.3-0.38	0.21-0.26 (vulva-anus)	0.22-0.315	0.17-0.21
Anus-tail	0.08-0.09	0.053	0.07-0.1	0.075-0.09	0.061-0.1	0.062-0.075

	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17
1. Ancylostoma duodenale (AJ417718)
2. Necator americanus (AJ417719)
3. Protostrongylus rufescens (NC_023262)	37.240
4. Metastrongylus pudendotectus (NC013813)	38.343	35.950
5. Metastrongylus salmi (NC013815)	45.664	42.342	20.002
6. Parafilaroides normani (NC024656)	24.342	30.736	31.055	35.661
7. Heterostrongylus heterostrongylus (Ilha Grande, RJ)	27.033	34.833	32.439	35.547	25.143
8. Heterostrongylus heterostrongylus (PEPB/CFMA, RJ)	26.825	34.858	32.315	35.627	24.855	0.007
9. Aelurostrongylus abstrusus (NC019571)	27.617	28.646	37.879	31.581	20.158	20.917	20.834
10. Angiostrongylus cantonensis (GQ398121)	25.772	36.751	37.191	36.876	27.641	21.953	22.020	23.555
11. Angiostrongylus malaysiensis (KT947979)	31.707	35.441	39.113	38.985	30.821	24.849	24.834	26.821	6.851
12. Angiostrongylus chabaudi (KU521521)	31.619	37.349	43.042	40.547	30.834	31.075	31.107	28.164	20.284	19.502
13. Angiostrongylus vasorum (GQ982735)	30.756	37.879	37.246	38.593	23.388	28.032	27.959	24.266	21.889	23.614	14.273
14. Angiostrongylus vasorum (GQ982871)	30.804	37.872	37.293	38.587	23.386	28.078	28.006	24.315	21.886	23.610	14.326	0.003
15. Angiostrongylus costaricensis (GQ398122)	30.033	37.828	36.428	30.768	26.478	21.172	21.296	20.626	20.013	21.170	21.327	18.523	18.520
16. Angiostrongylus costaricensis (KR827449)	29.261	30.774	33.170	27.778	26.751	23.981	24.094	20.862	19.454	19.216	27.288	21.502	21.499	13.280
17. Angiostrongylus costaricensis (KX378965)	30.746	38.294	37.080	36.371	28.946	23.149	23.103	25.270	17.715	17.172	16.790	16.262	16.258	16.172	17.539
*18. Angiostrongylus minasensis* n. sp.**	30.828	37.776	35.207	35.380	28.988	23.065	22.832	25.307	19.866	18.284	17.989	17.007	17.003	18.439	17.466	0.233

[1] *Corresponding author: Walter dos Santos Lima. E-mail: wlima@icb.ufmg.br

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Angiostrongylus minasensis n. sp.: nova espécie encontrada parasitando quatis (Nasua nasua) em área de proteção urbana no Brasil

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