A new species of <i>Huffmanela</i> (Nematoda: Trichosomoididae) parasitizing <i>Colomesus psittacus</i> (Tetraodontiformes) from Marajó Island, Pará State, Brazil

Carvalho, Elaine Lopes de; Santana, Ricardo Luis Sousa; Corrêa, Gilson Campos; Sindeaux Neto, José Ledamir; Pinheiro, Raul Henrique da Silva; Giese, Elane Guerreiro

doi:10.1590/S1984-29612022045

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Revista Brasileira de Parasitologia Veterinária

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Original Article • Rev. Bras. Parasitol. Vet. 31 (3) • 2022 • https://doi.org/10.1590/S1984-29612022045 copy

A new species of Huffmanela (Nematoda: Trichosomoididae) parasitizing Colomesus psittacus (Tetraodontiformes) from Marajó Island, Pará State, Brazil

Uma nova espécie de Huffmanela (Nematoda: Trichosomoididae) parasitando Colomesus psittacus (Tetraodontiformes) da Ilha de Marajó, Pará, Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The puffer fish Colomesus psittacus, is not commercialized on Marajó Island. They are captured as bycacth and discarded dead in the environment in artisanal fisheries that occur in the estuaries of northern Brazil. In this sense, the objective was to identify the parasites present in the gills and to evaluate the histopathological alterations caused by these nematodes of the genus Huffmanela. Fifty-five fish were analyzed, and thirty-five specimens showed the parasite in the gills. Morphological characteristics suggest that it is a new species of the genus Huffmanela, and the histopathological exams showed an edematous inflammation in the secondary lamella and the presence of eggs of this nematode, which is the first record of this parasite in C. psittacus in Brazil.

Keywords:
Trichosomoididae; Huffmanela; Pisces; Tetraodontiformes; Amazon

Morphometric characterization	Huffmanela psittacus n. sp.		H. huffmani		H. canadensis		H. moraveci		H. balista	H. longa
Specimen sex	Male	Female	Male	Female	Male	Female	Male	Female	Male	Female	Female
Host Locality	*Colomesus psittacus* Pará		Lepomis spp., Amblopites rupestris, Micropterus salmoides Texas, USA		Sebastes spp. Canada		Odontesthes smitti, O. nigricans Argentina		Abalistes stellatus New Caledonia	Gymnocranius grandoculis New Caledonia
Total body (TL) ^a	3.40–5.60	7.50–11.90	4.69–5.14	4.9–7.51	3.44–3.86	7.71–8.16	3.8–6.4	5–16.3	9.87	4.85	20.73
Maximum body (W) ^b	18.30–28.30	30–48.30	24–27	24–30	45–63	90–105	60–90	58–120	30	56	32
cephalic end (W) ^b	10.00–16.7	15–33.30	12	12	12	15–18	8–15	10–20	10	16	11
Nerve-ring (L) ^{b, c}	25.00–60.00	40–82	51–57	45–48	48–69	75–78	55–90	70–145	not seen	not seen	not seen
Total esophagus (L) ^a	1.00–2.00	1.50-2.30	1.39–1.90	1.29–2.31	1.33–1.34	1.76–2,05	1.15–1.6	1.35–2.35	3.89	1.98	6.72
Muscular esophagus (L) ^{a, c}	65–235	190–227	135–141	150–162	147–153	180–216	110–160	130–260	366	438	181
Muscular esophagus (W) ^b	6.7–18.3	10–18	–	–	–	–	–	–		8–9
Stichosome (L) ^a	1.10–1.90	1.30–2.10	1.25–1.76	1.14–2.15	1.18–1,19	1.56–1,83	1–1.5	1.2–2.1	3.52	–	6.51
# Stichocytes	28–43	32–35	25–26	29–35	36–42	32–37	25–37	30–42	25	–	35
Tail (L) ^b,d	3.30–8.30	20–73.3	6–7	–	–		–	–	–	–	–
Vulva (L) ^a,c	–	1.50–2.60^c	–	0.015–0.030^e	–	0.039^e	1.85^c	1.5–2.8^c	–	–	0.040^e
Eggs immature (L × W) ^d×d	–	28.3–33.3×16.6–23.3	–	45×27	–	36-39 × 24-27	–	38–55×23–30	–	41–44 × 17–21	–
Eggs mature (L×W) ^d×d	–	36.7–50×18.30–20	–	60–63×33–39	–	54×26	–	50–57×23–31	–	70.5×34.5	66×26.6
Oesophagus/TL (%)	30–41%	15–27%	29–41%	26–31%	39%	23%	24–32%	13–21%	39%	–	–
^# Specimen	22	10	10	5	2	3	9	11	1	1	1
Reference	In this study		Huffman & Moravec (1988)Huffman DG, Moravec F. First description of adult Huffmanela huffmani Moravec, 1987 (Nematoda: Trichosomoididae) from the swimbladder of centrarchid fishes of the upper San Marcos River, central Texas. Folia Parasitol (Praha) 1988; 35(3): 227-234.		Moravec et al. (2005)Moravec F, Conboy GA, Speare DJ. A new trichosomoidid from the skin of Sebastes spp. (Pisces) from British Columbia, Canada. J Parasitol 2005; 91(2): 411-414. http://dx.doi.org/10.1645/GE-3420. PMid:15986617. http://dx.doi.org/10.1645/GE-3420...		Carballo & Navone (2007)Carballo MC, Navone GT. A new Huffmanela species (Nematoda: Trichosomoididae) parasitizing atherinid fishes in north Patagonian gulfs, Argentina. J Parasitol 2007; 93(2): 377-382. http://dx.doi.org/10.1645/GE-971R.1. PMid:17539422. http://dx.doi.org/10.1645/GE-971R.1...		Justine (2007)Justine JL. Huffmanela spp. (Nematoda, Trichosomoididae) parasites in coral reef fishes off New Caledonia, with descriptions of H. balista n. sp. and H. longa n. sp. Zootaxa 2007; 1628(1-2): 23-41. http://dx.doi.org/10.11646/zootaxa.1628.1.2. http://dx.doi.org/10.11646/zootaxa.1628....	Justine (2007)Justine JL. Huffmanela spp. (Nematoda, Trichosomoididae) parasites in coral reef fishes off New Caledonia, with descriptions of H. balista n. sp. and H. longa n. sp. Zootaxa 2007; 1628(1-2): 23-41. http://dx.doi.org/10.11646/zootaxa.1628.1.2. http://dx.doi.org/10.11646/zootaxa.1628....

Morphometric characterization		Huffmanela psittacus n. sp.			H. huffmani		H. schouteni		H. japonica			H. shikokuensis		H. paronai
Host Locality		Colomesus psittacus Pará			Lepomis spp., Amblopites rupestris, Micropterus salmoides Texas, USA		Hirundichthys affinis, Cypselurus Netherlands antilles		Upeneus bensasi; Stephanolepis cirrhifer Japan			Stephanolepis spp. Japan		Xiphias gladius Western Mediterranean

Eggs immature (L×W) ^a		25.1–33.3×16.6–23.3			45×27		–		46×25			–		43–50×19–23
Eggs mature (L×W) ^a		46.7–51.7×21.7–25			60–63×33–39		69-75 × 27-30		58-69×26-30			78–90×36-45		48–51 × 21–24
Shell surface morphology		Longitudinal, oblique and transverse ridges			spinose		thin envelope with protuberances		spinose			grainy		smooth surface
Site of infection		gill arch, gills and gill-mucosa			swimbladder		serosa of intestine, abdominal cavity, swimbladde		muscle			muscle		Epidermis^b
Reference		In this study			Huffman & Moravec (1988)Huffman DG, Moravec F. First description of adult Huffmanela huffmani Moravec, 1987 (Nematoda: Trichosomoididae) from the swimbladder of centrarchid fishes of the upper San Marcos River, central Texas. Folia Parasitol (Praha) 1988; 35(3): 227-234.		Moravec & Campbell (1991)Moravec F, Campbell BG. A new Huffmanela species, H. schouteni sp. n. (Nematoda: Trichosomoididae) from flying fishes in Curaçao. Folia Parasitol (Praha) 1991; 38(1): 29-32. PMid:1916528.		Moravec et al. (1998)Moravec F, Koudela B, Ogawa K, Nagasawa K. Two new Huffmanela species, H. japonica n. sp. and H. shikokuensis n. sp. (Nematoda: Trichosomoididae), from marine fishes in Japan. J Parasitol 1998; 84(3): 589-593. http://dx.doi.org/10.2307/3284728. PMid:9645862. http://dx.doi.org/10.2307/3284728...			Moravec et al. (1998)Moravec F, Koudela B, Ogawa K, Nagasawa K. Two new Huffmanela species, H. japonica n. sp. and H. shikokuensis n. sp. (Nematoda: Trichosomoididae), from marine fishes in Japan. J Parasitol 1998; 84(3): 589-593. http://dx.doi.org/10.2307/3284728. PMid:9645862. http://dx.doi.org/10.2307/3284728...		Moravec & Garibaldi (2000)Moravec F, Garibaldi F. Huffmanela paronai sp. n. (Nematoda: Trichosomoididae), a new parasite from the skin of swordfish Xiphias gladius in the Ligurian Sea (Western Mediterranean). Folia Parasitol (Praha) 2000; 47(4): 309-313. http://dx.doi.org/10.14411/fp.2000.053. PMid:11151956. http://dx.doi.org/10.14411/fp.2000.053...
		Huffmanela psittacus n. sp.			H. mexicana		H. banningi		H. carcharini			Huffmanela spp.		H. schouteni
Host Locality		Colomesus psittacus Pará			Sphoeroides annulatus Mexico		Cynoglossus browni Atlantic Ocean, Senegal and Congo		Carcharhinus melanopterus, C. plumbeus Atlantic Ocean, USA			Sebastes spp. Canada		Cheilopogon heterurus Europe

Eggs immature (L × W) ^a		25.1–33.3×16.6–23.3			–		–		–			–		–
Eggs mature (L×W) ^a		46.7–51.7×21.7–25			63–69×30–33		99–108×42–45		90–105 × 42–54			50–55×21–27		69–75×30–33
Shell surface morphology		Longitudinal, oblique and transverse ridges			smooth surface		spinose		envelope visible at pole regions			Tranverse ridges		–
Site of infection		gill arch, gills and gill-mucosa			swimbladder		muscle		skins and mucosa of connective tissue of gill arches			skin		swimbladder
Reference		In this study			Moravec & Fajer-Avila (2000)Moravec F, Fajer-Avila E. Huffmanela mexicana n. sp. (Nematoda: Trichosomoididae) from the marine fish Sphoeroides annulatus in Mexico. J Parasitol 2000; 86(6): 1229-1231. http://dx.doi.org/10.1645/0022-3395(2000)086[1229:HMNSNT]2.0.CO;2. PMid:11191896. http://dx.doi.org/10.1645/0022-3395(2000...		Moravec (2001)Moravec F. Trichinelloid nematodes parasitic in cold-blooded vertebrates. Praha, Czech Republic: Academia; 2001.		Moravec (2001)Moravec F. Trichinelloid nematodes parasitic in cold-blooded vertebrates. Praha, Czech Republic: Academia; 2001.			Conboy & Speare (2002)Conboy GA, Speare DJ. Dermal nematodosis in commercially captured rockfish (Sebastes spp.) from coastal British Columbia, Canada. J Comp Pathol 2002; 127(2-3): 211-213. http://dx.doi.org/10.1053/jcpa.2002.0567. PMid:12354534. http://dx.doi.org/10.1053/jcpa.2002.0567...		Moravec & Garibaldi (2003)Moravec F, Garibaldi F. First record of Huffmanela schouteni (Nematoda: Trichosomoididae), a histozoic parasite of flyingfishes, in Europe. Dis Aquat Organ 2003; 57(1-2): 173-175. http://dx.doi.org/10.3354/dao057173. PMid:14735938. http://dx.doi.org/10.3354/dao057173...

Morphometric characterization	Huffmanela psittacus n. sp.			H. filamentosa		H. branchialis		H. ossicola		Huffmanela sp.			H. lata
Host Locality	Colomesus psittacus Pará			Gymnocranius grandoculis New Caledonia		Nemipterus furcosus New Caledonia		Bodianus loxozonus B. perditio, B. busellatus New Caledonia		Pentapodus aureofasciatus New Caledonia			Carcharhinus amblyrhynchos Pacific Ocean, New Caledonia

Eggs immature (L × W) ^a	25.1–33.3×16.6–23.3			–		–		–		–			–
Eggs mature (L×W) ^a	46.7–51.7×21.7–25			48–53×25–30		45–52×23–30		72–88 × 32–40		39–47 × 22–27			77–88 × 52–63
Shell surface morphology	Longitudinal, oblique and transverse ridges			filaments at extremities		aspinose		numerous filaments on eggs surrounded by thin envelope		no filaments			spinose
Site of infection	gill arch, gills and gill-mucosa			gill–mucosa		gills-filaments		within all bones, including gill arch bones		mucosa of gills			skin
Reference	In this study			Justine (2004)Justine JL. Three new species of Huffmanela Moravec, 1987 (Nematoda: Trichosomoididae) from the gills of marine fish off New Caledonia. Syst Parasitol 2004; 59(1): 29-37. http://dx.doi.org/10.1023/B:SYPA.0000038442.25230.8b. PMid:15318018. http://dx.doi.org/10.1023/B:SYPA.0000038...		Justine (2004)Justine JL. Three new species of Huffmanela Moravec, 1987 (Nematoda: Trichosomoididae) from the gills of marine fish off New Caledonia. Syst Parasitol 2004; 59(1): 29-37. http://dx.doi.org/10.1023/B:SYPA.0000038442.25230.8b. PMid:15318018. http://dx.doi.org/10.1023/B:SYPA.0000038...		Justine (2004)Justine JL. Three new species of Huffmanela Moravec, 1987 (Nematoda: Trichosomoididae) from the gills of marine fish off New Caledonia. Syst Parasitol 2004; 59(1): 29-37. http://dx.doi.org/10.1023/B:SYPA.0000038442.25230.8b. PMid:15318018. http://dx.doi.org/10.1023/B:SYPA.0000038...		Justine (2004)Justine JL. Three new species of Huffmanela Moravec, 1987 (Nematoda: Trichosomoididae) from the gills of marine fish off New Caledonia. Syst Parasitol 2004; 59(1): 29-37. http://dx.doi.org/10.1023/B:SYPA.0000038442.25230.8b. PMid:15318018. http://dx.doi.org/10.1023/B:SYPA.0000038...			Justine (2005)Justine JL. Huffmanela lata n. sp. (Nematoda: Trichosomoididae: Huffmanelinae) from the shark Carcharhinus amblyrhynchos (Elasmobranchii: Carcharhinidae) off New Caledonia. Syst Parasitol 2005; 61(3): 181-184. http://dx.doi.org/10.1007/s11230-005-3160-8. PMid:16025207. http://dx.doi.org/10.1007/s11230-005-316...

	Huffmanela psittacus n. sp.			Huffmanela sp.		H. canadensis		H. moraveci		H. balista			H. longa
Host Locality	Colomesus psittacus Pará			Carcharhinus plumbeus North Carolina, USA		Sebastes spp. Canada		Odontesthes smitti, O. nigricans Argentina		Abalistes stellatus New Caledonia			Gymnocranius grandoculis New Caledonia

Eggs immature (L × W) ^a	25.1–33.3×16.6–23.3			–		36–39 × 24–27		26–44×21–28		–			–
Eggs mature (L×W) ^a	46.7–51.7×21.7–25			73–86 × 39–47		48–63 × 26 24–27		50–57×23–31		63–78 × 32–41			58–69 × 26–34
Shell surface morphology	Longitudinal, oblique and transverse ridges			–		numerous transverse and somewhat oblique, complete or incomplete ridges		lightly ornamented		no filament			long thin filaments at eggs extremities
Site of infection	gill arch, gills and gill-mucosa			skin		skin		skin and gills		outer swimbladder wall			mesentery, mucosa of abdominal cavity, outer Swimbladder wall
Reference	In this study			MacLean et al. (2006)MacLean RA, Fatzinger MH, Woolard KD, Harms CA. Clearance of a dermal Huffmanela sp. in a sandbar shark (Carcharhinus plumbeus) using levamisole. Dis Aquat Organ 2006; 73(1): 83-88. http://dx.doi.org/10.3354/dao073083. PMid:17240757. http://dx.doi.org/10.3354/dao073083...		Moravec et al. (2005)Moravec F, Conboy GA, Speare DJ. A new trichosomoidid from the skin of Sebastes spp. (Pisces) from British Columbia, Canada. J Parasitol 2005; 91(2): 411-414. http://dx.doi.org/10.1645/GE-3420. PMid:15986617. http://dx.doi.org/10.1645/GE-3420...		Carballo & Navone (2007)Carballo MC, Navone GT. A new Huffmanela species (Nematoda: Trichosomoididae) parasitizing atherinid fishes in north Patagonian gulfs, Argentina. J Parasitol 2007; 93(2): 377-382. http://dx.doi.org/10.1645/GE-971R.1. PMid:17539422. http://dx.doi.org/10.1645/GE-971R.1...		Justine (2007)Justine JL. Huffmanela spp. (Nematoda, Trichosomoididae) parasites in coral reef fishes off New Caledonia, with descriptions of H. balista n. sp. and H. longa n. sp. Zootaxa 2007; 1628(1-2): 23-41. http://dx.doi.org/10.11646/zootaxa.1628.1.2. http://dx.doi.org/10.11646/zootaxa.1628....			Justine (2007)Justine JL. Huffmanela spp. (Nematoda, Trichosomoididae) parasites in coral reef fishes off New Caledonia, with descriptions of H. balista n. sp. and H. longa n. sp. Zootaxa 2007; 1628(1-2): 23-41. http://dx.doi.org/10.11646/zootaxa.1628.1.2. http://dx.doi.org/10.11646/zootaxa.1628....
Morphometric characterization	Huffmanela psittacus n. sp.		Huffmanela sp.			H. plectropomi		H. carcharhini			H. oleumimica		H. markgracei
Host Locality	Colomesus psittacus Pará		Trisopterus luscus Portuguese coast			Plectropomus leopardus New Caledonia		Carcharhinus plumbeus Pacific Ocean			Lutjanus campechanus Northern Gulf of Mexico		Rhizoprionodon terraenovae Gulf of Mexico

Eggs immature (L × W) ^a	25.1–33.3×16.6–23.3		33–57×26–38			–		–			47–53×26–32		97–109×40–44
Eggs mature (L×W) ^a	46.7–51.7×21.7–25		73–94×39–59			64–76×29–35		75–95×48–63			160–201×7–8		90–113×39–54 99–109×39-49
Shell surface morphology	Longitudinal, oblique and transverse ridges		–			filaments		spinose			spinose		transverse ridges
Site of infection	gill arch, gills and gill-mucosa		Muscle, skin, mucosa intestine, swimbladder			mesentery		skin			epidermis of urohyal, branchiostegals, and buccal cavity		skin of tongue, branchial arches and buccal cavity
Reference	In this study		Esteves et al. (2009)Esteves A, Seixas F, Carvalho S, Nazário N, Mendes M, Martins C. Huffmanela sp. (Nematoda: Trichosomoididae) muscular parasite from Trisopterus luscus captured off the Portuguese coast. Dis Aquat Organ 2009; 84(3): 251-255. http://dx.doi.org/10.3354/dao02048. PMid:19565703. http://dx.doi.org/10.3354/dao02048...			Justine (2011)Justine JL. Huffmanela plectropomi n. sp. (Nematoda: Trichosomoididae: Huffmanelinae) from the coralgrouper Plectropomus leopardus (Lacépède) off New Caledonia. Syst Parasitol 2011; 79(2): 139-143. http://dx.doi.org/10.1007/s11230-011-9296-9. PMid:21544712. http://dx.doi.org/10.1007/s11230-011-929...		Bullard et al. (2012)Bullard SA, Ruiz CF, McElwain A, Murray MJ, Borucinska JD, Benz GW. Huffmanela cf. carcharhini (Nematoda: Trichosomoididae: Huffmanelinae) from skin of a sandbar shark, Carcharhinus plumbeus, in the Pacific Ocean. J Parasitol 2012; 98(2): 333-340. http://dx.doi.org/10.1645/GE-2962.1. PMid:22032442. http://dx.doi.org/10.1645/GE-2962.1...			Ruiz et al. (2013)Ruiz CF, Ray CL, Cook M, Grace MA, Bullard SA. A New Species of Trichosomoididae (Nematoda) from Skin of Red Snapper, Lutjanus campechanus (Perciformes: Lutjanidae) on the Texas–Louisiana Shelf, Northern Gulf of Mexico. J Parasitol 2013; 99(2): 318-326. http://dx.doi.org/10.1645/GE-3249.1. PMid:22985426. http://dx.doi.org/10.1645/GE-3249.1...		Ruiz & Bullard (2013)Ruiz CF, Bullard SA. Huffmanela markgracei sp. n. (Nematoda: Trichosomoididae) from buccal cavity of Atlantic sharpnose shark, Rhizoprionodon terraenovae (Carcharhiniformes: Carcharhinidae), in the northwestern Gulf of Mexico off Texas. Folia Parasitol (Praha) 2013; 60(4): 353-358. http://dx.doi.org/10.14411/fp.2013.036. PMid:24261136. http://dx.doi.org/10.14411/fp.2013.036...

	Huffmanela psittacus n. sp.		H. hamo			Huffmanela spp.		H. lusitana			Huffmanela sp.		Huffmanela sp.
Host Locality	Colomesus psittacus Pará		Muraenesox cinereus Japan			Microchirus azevia Coast atlantic		Trisopterus luscus Atlantic coast of Portugal			Carcharhinus dussumieri Saudi Arabia		Epinephelus coioides Saudi Arabia

Eggs immature (L × W) ^a	25.1–33.3×16.6–23.3		66–77×33–38			47–51×26–32		39.7–59.1×22–36.8			92–110×35–48		60.3–75.6×26.4–36.5
Eggs mature (L×W) ^a	46.7–51.7×21.7–25		70–79×34–39			75–86×37–42		69.1–82.9×36.9–45.7			95–107×34–49		–
Shell surface morphology	Longitudinal, oblique and transverse ridges		smooth			–		smooth			filaments or ridges		–
Site of infection	gill arch, gills and gill-mucosa		muscle			Muscle, gill arch, skin		Epaxial and hypaxial musculature			skin		muscle
Reference	In this study		Justine & Iwaki (2014)Justine JL, Iwaki T. Huffmanela hamo sp. n. (Nematoda: Trichosomoididae: Huffmanelinae) from the dagger-tooth pike conger Muraenesox cinereus off Japan. Folia Parasitol (Praha) 2014; 61(3): 267-271. http://dx.doi.org/10.14411/fp.2014.029. PMid:25065133. http://dx.doi.org/10.14411/fp.2014.029...			Esteves et al. (2016)Esteves A, Oliveira I, Ramos P, Carvalho A, Nazário N, Seixas F. Huffmanela spp. (Nematoda, Trichosomoididae) from Microchirus azevia: tissue location and correspondence of host muscle discoloration with parasite burden. J Fish Aquat Sci 2016; 11(4): 304-310. https://dx.doi.org/10.3923/jfas.2016.304.310. https://dx.doi.org/10.3923/jfas.2016.304...		Ramos et al. (2019)Ramos P, Carvalho R, Rosa F, Alexandre-Pires G, Seixas F, Esteves A, et al. Huffmanela lusitana sp. n. (Nematoda: Trichosomoididae) infecting pouting, Trisopterus luscus (Teleostei: Gadidae) off the Atlantic coast of Portugal. Int J Parasitol Parasites Wildl 2019; 9: 266-273. http://dx.doi.org/10.1016/j.ijppaw.2019.05.010. PMid:31245277. http://dx.doi.org/10.1016/j.ijppaw.2019....			Attia et al. (2021a)Attia MM, Ibrahim MM, Mahmoud MA, Al-Sabi MNS. Huffmanela sp. (Nematoda: Trichosomoididae: Huffmanelinae) encountered in the whitecheek shark (Carcharhinus dussumieri) in the Arabian Gulf. Helminthologia 2021a; 58(3): 281-291. http://dx.doi.org/10.2478/helm-2021-0030. PMid:34934391. http://dx.doi.org/10.2478/helm-2021-0030...		Attia et al. (2021b)Attia MM, Mahmoud MA, Ibrahim MM. Morphological and pathological appraisal of Huffmanela sp. (Nematoda: Trichosomoididae) infecting orange-spotted grouper (Epinephelus coioides, Hamilton, 1822) at Jubail Province, Saudi Arabia: a case report. J Parasit Dis 2021b; 45(4): 980-985. http://dx.doi.org/10.1007/s12639-021-01394-x. PMid:34789981. http://dx.doi.org/10.1007/s12639-021-013...

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[1] *Corresponding author: Elaine Lopes de Carvalho. E-mail: lheaufra@gmail.com