Molecular Detection and Distribution of Giardia duodenalis and Cryptosporidium spp. Infections in Wild and Domestic Animals in Portugal

Table 1

Prevalence and molecular diversity of Giardia duodenalis, Cryptosporidium spp., and Balantioides coli reported in the wild carnivores and ungulates in Europe.

Pathogen	Host scientific name	Country	Occurrence rate (no. pos./total no.)	Detection method	Locus	Species/genotype (n)	Subgenotype (n)	Reference
Wild carnivores
Giardia duodenalis	Canis lupus	Croatia	10 (13/127)	CM, PCR	ssu-rRNA, ITS1-ITS2, tpi, tpi-D^2	A (6), C (2), D (1), A + B + D (1), A + C + D (1), C + D (1)	A1^3 (6)	Beck et al. [25]
		Poland	29 (2/7)	CM, PCR	bg	D (2)	–	Stojecki et al. [26]
		Romania	100 (3/3)	PCR^1	gdh	D (3)	–	Adriana et al. [27]
		Italy	5 (1/20)	PCR	ssu-rRNA	C (1)	–	Di Francesco et al. [28]
		Italy	100 (1/1)	PCR^1	ssu-rRNA	D (1)	–	Guadano Procesi et al. [29]
	C. lupus signatus	Spain	17 (1/6)	PCR	gdh	NA	–	Mateo et al. [30]
		Portugal	26 (31/121)	PCR	ssu-rRNA, gdh, bg, tpi	D (4), C + D (2)	–	This study
	Lynx pardinus	Portugal	27 (8/30)	PCR	ssu-rRNA, gdh, bg, tpi	NA	NA	This study
	Vulpes vulpes	Norway	5 (13/269)	CM, PCR	gdh, bg	A (5), B (2)	A1^3 (2), A2^3 (1), B3^3 (1)	Hamnes et al. [31]
		Croatia	5 (3/66)	CM, PCR	ssu-rRNA, ITS1-ITS2, tpi, tpi-D^2	A (1)	NA	Beck et al. [25]
		Romania	5 (10/217)	PCR	bg	A (2), B (1)	AII (2)	Onac et al. [32]
		Sweden	44 (46/104)	CM, PCR	gdh, bg, tpi	B (4)	NA	Debenham et al. [33]
		Spain	8 (7/87)	PCR	gdh	NA	NA	Mateo et al. [30]
		Spain	10 (19/197)	PCR	ssu-rRNA, gdh, bg	NA	NA	Barrera et al. [34]
		Portugal	19 (22/118)	PCR	ssu-rRNA, gdh, bg, tpi	C + D (1)	–	This study
	Martes foina	Spain	13 (1/8)	PCR	gdh	NA	NA	Mateo et al. [30]
		Portugal	16 (3/19)	PCR	ssu-rRNA, gdh, bg, tpi	NA	NA	This study
Cryptosporidium spp.	Canis lupus	Poland	36 (5/14)	CM, PCR	cowp	C. parvum genotype 2 (5)	NA	Paziewska et al. [35]
		Czech Republic	6 (1/17)	CM, PCR	ssu-rRNA, actin, gp60	C. ubiquitum (1)	XIId (1)	Kváč et al. [36]
		Slovakia	4 (3/83)	CM, PCR	ssu-rRNA, actin, gp60	C. canis (2), C. ubiquitum (1)	XIId (1)	Kváč et al. [36]
		Slovakia	ND (4/ND)	PCR	ND	C. scrofarum (4)	–	Valenčáková et al. [37]
	C. lupus signatus	Portugal	3 (3/121)	PCR	ssu-rRNA, gp60	C. canis (3)	NA	This study
	Lynx pardinus	Portugal	3 (1/30)	PCR	ssu-rRNA	C. felis (1)	–	This study
	Vulpes vulpes	Ireland	20 (2/10)	CM, PCR	ssu-rRNA, gp60	C. parvum (2)	Ic (1), II (1)	Nagano et al. [38]
		Spain	8 (7/87)	PCR	ssu-rRNA	C. parvum (3), C. canis (2), C. felis (1), C. ubiquitum (1)	NA	Mateo et al. [30]
		Spain	6 (12/197)	PCR	ssu-rRNA, gp60	C. hominis (4), C. canis (3), C. parvum (2), C. ubiquitum (1), C. suis (1), Cryptosporidium spp. (1)	NA	Barrera et al. [34]
		Czech Republic	2 (1/58)	CM, PCR	ssu-rRNA, actin, gp60	C. tyzzeri (1)	IXa (1)	Kváč et al. [36]
		Poland	3 (2/74)	CM, PCR	ssu-rRNA, actin, gp60	C. andersoni (2)	–	Kváč et al. [36]
		Poland	12 (6/50)	PCR	ssu-rRNA, actin	C. canis (3), C. alticolis (2), C. vole genotype II (1)	–	Perec-Matysiak et al. [39]
		Slovakia	2 (1/47)	CM, PCR	ssu-rRNA, actin, gp60	C. galli (1)	–	Kváč et al. [36]
		Portugal	3 (4/118)	PCR	ssu-rRNA, gp60	C. canis (4)	NA	This study
	Martes foina	Poland	29 (15/51)	PCR	ssu-rRNA, actin	C. ditrichi (15)	–	Perec-Matysiak et al. [39]
Wild ungulates
Giardia duodenalis	Cervus elaphus	Croatia	1 (4/374)	CM, PCR	ssu-rRNA, ITS1-5.8S-ITS2, tpi, tpi-D^2	A (4), D (1)	A1^3 (2), A3^3 (1)	Beck et al. [25]
		Poland	2 (1/61)	CM, PCR	gdh, bg, tpi	A (1)	AIII (1)	Solarczyk et al. [40]
		Poland	18 (5/28)	CM, PCR	bg	B (4)	NA	Stojecki et al. [26]
		Spain	2 (8/329)	PCR	ssu-rRNA, gdh, bg, tpi	NA	NA	Dashti et al. [41]
		Portugal	4 (4/96)	PCR	ssu-rRNA, gdh, bg, tpi	NA	NA	This study
	Capreolus capreolus	The Netherlands	100 (1/1)	PCR^1	ssu-rRNA, gdh	A (1)	NA	van der Giessen et al. [42]
		Croatia	24 (5/21)	CM, PCR	ssu-rRNA, ITS1-5.8S-ITS2, tpi, tpi-D^2	A (2), C (1), D (2)	A1^3 (1), A3^3 (1)	Beck et al. [25]
		Poland	4 (2/50)	CM, PCR	gdh, bg, tpi	A (2)	AI (2)	Solarczyk et al. [40]
		Poland	23 (11/48)	CM, PCR	bg	B (8)	NA	Stojecki et al. [26]
		Spain	9 (19/212)	CM, PCR	bg	A (7)	AII (7)	García-Presedo et al. [43]
		Spain	8 (7/93)	PCR	ssu-rRNA, gdh, bg, tpi	NA	NA	Dashti et al. [41]
		Romania	100 (4/4)	PCR^1	gdh	E (4)	–	Adriana et al. [27]
		Portugal	10 (4/39)	PCR	ssu-rRNA, gdh, bg, tpi	A (1)	AI (1)	This study
	Sus scrofa	Croatia	1 (2/144)	CM, PCR	ssu-rRNA, ITS1-5.8S-ITS2, tpi, tpi-D^2	A (1)	A3^3 (1)	Beck et al. [25]
		Poland	41 (11/27)	CM, PCR	bg	B (6)	NA	Stojecki et al. [26]
		Spain	23 (32/142)	PCR	gdh, bg, tpi	NA	NA	Rivero-Juarez et al. [44]
		Spain	6 (20/359)	PCR	ssu-rRNA, gdh, bg, tpi	A (1)	NA	Dashti et al. [41]
		Spain	1 (6/498)	PCR	ssu-rRNA, gdh, bg	E (1)	NA	Martí-Marco et al. [45]
		Italy	100 (4/4)	PCR^1	ssu-rRNA, gdh, bg, tpi	A (4), D (1)	AI (2), AII (2)	Guadano Procesi et al. [29]
		Portugal	15 (16/107)	PCR	ssu-rRNA, gdh, bg, tpi	E (1)	–	This study
Cryptosporidium spp.	Cervus elaphus	Czech Republic	100 (1/1)	PCR^1	ssu-rRNA, cowp	C. parvum (1)	–	Hajdušek et al. [46]
		Poland	4 (6/136)	CM, PCR	ssu-rRNA, gp60	C. ubiquitum (5), C. muris (1)	XIId (5)	Kotková et al. [47]
		Spain	3 (9/329)	PCR	ssu-rRNA, gp60	C. ryanae (7), C. parvum (1), C. suis (1)	NA	Dashti et al. [41]
		Portugal	3 (3/96)	PCR	ssu-rRNA, gp60	C. ubiquitum (1), C. ryanae (1), C. suis (1)	NA	This study
	Capreolus capreolus	Spain	4 (9/212)	CM, PCR	ssu-rRNA	C. bovis (3), C. ryanae (3)	–	García-Presedo et al. [43]
		Spain	8 (7/93)	PCR	ssu-rRNA, gp60	C. ryanae (5), C. ubiquitum (1), C. canis (1)	NA	Dashti et al. [41]
		Italy	4 (4/119)	CM, PCR	cowp, gp60	C. ubiquitum (4)	NA	Trogu et al. [48]
	Sus scrofa	Czech Republic	17 (32/193)	CM, PCR	ssu-rRNA	C. suis (18), C. scrofarum^3 (7), C. suis/C. scrofarum^4 (12)	–	Němejc et al. [49]
		Czech Republic	17 (39/231)	CM, PCR	ssu-rRNA, gp60	C. scrofarum (14), C. suis (13), C. suis/C. scrofarum (12)	–	Němejc et al. [49]
		Austria	18 (8/44)	CM, PCR	ssu-rRNA, gp60	C. suis (2), C. scrofarum (1), C. suis/C. scrofarum (2)	–	Němejc et al. [49]
		Poland	9 (11/129)	CM, PCR	ssu-rRNA, gp60	C. scrofarum (8), C. suis (1), C. suis/C. scrofarum (2)	–	Němejc et al. [49]
		Slovak Republic	5 (3/56)	CM, PCR	ssu-rRNA, gp60	C. suis (2), C. scrofarum (1)	–	Němejc et al. [49]
		Slovakia	ND (3/ND)	PCR	ND	C. scrofarum (1), C. suis (2)	–	Valenčáková et al. [37]
		Spain	17 (35/209)	CM, PCR	ssu-rRNA, gp60	C. scrofarum (19), C. suis (5), C. parvum (3)	IIa (3)	García-Presedo et al. [50]
		Spain	6 (9/142)	PCR	ssu-rRNA	C. scrofarum (8), C. suis (1)	–	Rivero-Juarez et al. [44]
		Spain	7 (25/359)	PCR	ssu-rRNA, gp60	C. scrofarum (22), C. ryanae (1), C. parvum (1), Cryptosporidium spp. (1)	NA	Dashti et al. [41]
		Spain	22 (108/498)	PCR	ssu-rRNA	C. scrofarum (94), C. suis (14)	NA	Martí-Marco et al. [45]
		Portugal	1 (2/144)	PCR	ssu-rRNA	C. scrofarum (2)	–	Santos-Silva et al. [51]
		Portugal	8 (9/107)		ssu-rRNA, gp60	C. ubiquitum (1), C. scrofarum (8)	NA	This study
Balantioides coli	Cervus elaphus	Portugal	4 (4/95)	PCR	ITS	A (2), B (2)	–	Mega et al. [52]
	Sus scrofa	Czech Republic	100 (1/1)	PCR^1	ITS	A (1)	–	Pomajbíková et al. [53]
		Spain	12 (16/142)	PCR	ITS	NA	–	Rivero-Juarez et al. [44]
		Spain	3 (9/359)	PCR	ITS	NA	–	Dashti et al. [41]
		Portugal	15 (21/144)	PCR	ITS	A (16), B (5)	–	Santos-Silva et al. [51]

Note. bg, β-giardin; CM, conventional microscopy; cowp, Cryptosporidium oocyst wall protein; gdh, glutamate dehydrogenase; gp60, 60-kDa glycoprotein; ITS, internal transcribed spacer; NA, no amplification; ND, no data available; PCR, polymerase chain reaction; ssu-rRNA, small subunit ribosomal RNA; tpi, triose phosphate isomerase. ¹PCR conducted only in samples with a previous positive result by another detection method. ²Primer sequences specifically designed to amplify assemblage D. ³Previous nomenclature adopted by the authors. ⁴Formerly known as Cryptosporidium pig genotype II.