Epidemiology of <i>Giardia duodenalis</i> assemblages in Brazil: there is still a long way to go

Giardia duodenalis infection is distributed worldwide and can achieve prevalence around 60%, especially in developing countries. This protozoan is divided into eight assemblages, in which A and B have high zoonotic potential, whereas C to H are host-specific. This scenario is changing as molecular studies progress, highlighting that knowledge on host-specificity still has a long way to go. Understanding the players involved in transmission routes enables rational designs of control strategies. Considering the high prevalence of giardiasis, this review aims to gather together the data on available studies on the distribution of G. duodenalis assemblages in Brazil until September 2020.

Key words:
Giardia duodenalis; assemblage; genotyping; human; animals; water and soil; Brazil

Authorship

Maria Fantinatti ⁺+ Corresponding author: fantinatti@ioc.fiocruz.br

Fundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Laboratório Interdisciplinar de Pesquisas Médicas, Rio de Janeiro, RJ, BrasilFundação Oswaldo Cruz-FiocruzBrazilRio de Janeiro, RJ, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Laboratório Interdisciplinar de Pesquisas Médicas, Rio de Janeiro, RJ, Brasil

https://orcid.org/0000-0001-6485-6893

Monique Gonçalves-Pinto

Luiz Antonio Pimentel Lopes-Oliveira

Alda Maria Da-Cruz

Universidade do Estado do Rio de Janeiro, Faculdade de Ciências Médicas, Rio de Janeiro, RJ, BrasilUniversidade do Estado do Rio de JaneiroBrazilRio de Janeiro, RJ, BrazilUniversidade do Estado do Rio de Janeiro, Faculdade de Ciências Médicas, Rio de Janeiro, RJ, Brasil

+ Corresponding author: fantinatti@ioc.fiocruz.br

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables

Figures (3)
Tables (2)

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Fig. 1:
methodological search strategy for Medline bibliographic survey on Giardia duodenalis assemblages in Brazil.

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Fig. 2:
articles published on Medline about Giardia assemblage from Brazil. The points represent the number of published articles found in the search.

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Fig. 3:
distribution of Giardia duodenalis assemblage in Brazil. The states where G. duodenalis genotyping were not found are presented whithout colour. The arrows indicate the hosts and the respective assemblages observed.

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TABLE I
Genotyping studies of Giardia duodenalis in Brazil up to September 2020

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TABLE II
Giardia duodenalis assemblages found in animals and in the environment in Brazilian states

Fig. 1: methodological search strategy for Medline bibliographic survey on Giardia duodenalis assemblages in Brazil.

Fig. 2: articles published on Medline about Giardia assemblage from Brazil. The points represent the number of published articles found in the search.

Fig. 3: distribution of Giardia duodenalis assemblage in Brazil. The states where G. duodenalis genotyping were not found are presented whithout colour. The arrows indicate the hosts and the respective assemblages observed.

TABLE I Genotyping studies of Giardia duodenalis in Brazil up to September 2020

Year	Author	State	Isolate origin	Genotyping tool	Assemblage found
Year	Author	State	Isolate origin	Genotyping tool	βg	gdh	tpi	SSU-rRNA	orfC4
2020	Pineda et al.	São Paulo	Pool water	Sequencing	A	NI	NI	NI
2020	Corrêa et al.	São Paulo	Human	Sequencing	A, B	A, B	A, B
2019	de Aquino et al.	São Paulo	Buffalo	Sequencing	E	E	E	E
	Yamashiro et al.	São Paulo	Water	Sequencing	NI	NI	A	NI
	Yamashiro et al.	São Paulo	Sewage	Sequencing	B	NI	C	NI
	Pacheco et al.	Bahia	Human	PCR-RFLP	A, B	A, B
	Pacheco et al.	Bahia	Human	Sequencing	A, B
2018	Fantinatti et al.	Rio de Janeiro	Dog	Sequencing	A	A
	Ferreira et al.	Paraná	Vegetable	Sequencing		E	NI	NI
			Soil	Sequencing		E	NI	NI
			Water	Sequencing		E	NI	NI
	Seguí et al.	Paraná	Human	Sequencing	A	A, B
	De Araújo et al.	São Paulo	Surface raw water	qPCR (taqman)		A
	Leal et al.	São Paulo	Oyster	Sequencing			A
	Leal et al.	São Paulo	Estuarine water	Sequencing			A, C
	Nunes et al.	Amazonas	Human	Sequencing	A, B	A, B	A, B
		Ceará	Human	Sequencing	A, B	NI	NI
		Piauí	Human	Sequencing	A, B	A, B	A, B
2017	Rafael et al.	Paraná	Vegetable	PCR-RFLP		A, B, E
	Faria et al.	Rio de Janeiro	Human	Sequencing	A, B	A, B	A, B
	Da Cunha et al.	Minas Gerais	Toco toucan	Sequencing				A
2016	Ulloa-Stanojlović et al.	São Paulo	Wastewater	PCR (assemblage-specific)		A, B
	Fantinatti et al.	Rio de Janeiro	Human	Sequencing	A, E	A, E
	Quadros et al.	Santa Catarina	Human	PCR-RFLP		A, B
	Quadros et al.	Santa Catarina	Dog	PCR-RFLP		A, B, C
	Faria et al.	Rio de Janeiro	Human	PCR-RFLP	A, B	A, B
	Faria et al.	Rio de Janeiro	Human	qPCR (assemblage-specific)		A, B	A, B		A, B
	Coronato Nunes et al.	Amazonas	Human	Sequencing	A, B
	Scalia et al.	Minas Gerais	Human	Sequencing	A, B, E	A, B	A, B
	Tiyo et al.	Paraná	Vegetable	Sequencing		A
	Fava et al.	Minas Gerais	Dog	Sequencing		D	A, B, C, E
	Oliveira-Arbex	São Paulo	Human	Sequencing	A, B	A, B	A, B
2015	Colli et al.	Paraná	Human	PCR-RFLP	A, B	A, B
	Colli et al.	Paraná	Human	Sequencing		A, B
	David et al	São Paulo	Human	Sequencing	A, B	A, B	A, B
	David et al	São Paulo	Dog	Sequencing	A, C, D	A, C, D	A, C
	Colli et al.	Paraná	Human	PCR-RFLP	A, B	A, B
			Human	Sequencing		A, B
			Dog	PCR-RFLP	NI	NI
			Dog	Sequencing		B, C, D
			Vegetable	PCR-RFLP	NI	NI
			Vegetable	Sequencing		B
2014	Durigan et al.	São Paulo	Human	Sequencing	A, B	A, B	A, B, C
			Cat	Sequencing		D	A,B
				PCR (assemblage-specific)			D
			Dog	Sequencing	D	D	A, B, C
			Dog	PCR (assemblage-specific)			C, D
			Cattle	Sequencing	E	E	A
			Water	Sequencing	NI	A,B,D	B,C
	Paz e Silva et al.	São Paulo	Sheep	PCR-RFLP		E
	Paz e Silva et al.	São Paulo	Sheep	Sequencing		E
	David et al.	São Paulo	Nonhuman primates	Sequencing		A	A
2013	Fava et al.	Minas Gerais	Cattle	Sequencing		E	A, B, E
			Pig	Sequencing		E	NI
			Sheep	Sequencing		E	E, B
2012	Santos et al.	Minas Gerais	Human	Sequencing		B
	Paz e Silva et al.	São Paulo	Cattle	Sequencing		A, E		A, E
	Paz e Silva et al.	São Paulo	Cattle	PCR-RFLP		A, E		-
	Paz e Silva et al.	São Paulo	Dog	Sequencing	C, D	C, D		-
	Paz e Silva et al.	São Paulo	Dog	PCR-RFLP	C, D	C, D		-
2011	Fernandes et al.	São Paulo	Water	Sequencing		A
	Fernandes et al.	São Paulo	Sewage	Sequencing		A, B
	Volotão et al.	São Paulo	Human	Sequencing	A
	Volotão et al.	São Paulo	Dog	Sequencing	A
	Gomes et al.	Minas Gerais	Human	PCR (assemblage-specific)				A
	Gomes et al.	Minas Gerais	Dog	PCR (assemblage-specific)				A
	Soares et al.	Uninformed	Jaguar	Sequencing		A		A
			Nonhuman primates	Sequencing		B		B
			Chinchilla	Sequencing		B		B
			Ostriches	Sequencing		B		B
2008	Volotão et al.	Santa Catarina	Nonhuman primates	Sequencing	A
2008	Kohli et al.	Ceará	Human	qPCR multiplex				A, B
2007	Souza et al.	São Paulo	Human	Sequencing		A, B
			Cat	Sequencing		A, F
			Dog	Sequencing		C, D
			Cattle	Sequencing		A, E
	Volotão et al	Rio de Janeiro	Human	Sequencing	A
			Human	PCR-RFLP	A
			Dog	Sequencing	A
			Dog	PCR-RFLP	A
			Cat	Sequencing	A
			Cat	PCR-RFLP	A

The studies were grouped by year of publication, authors, state where the study was carried out, the isolate origin, the tool for genotyping used and the assemblages found according to the gene target used. The hatched area represents a genetic target not used in the methodological strategy. NI: assemblage not identified by the study; hatch: gene targets not used in the methodological strategy; PCR-RFLP: polymerase chain reaction restriction fragment length polymorphism; qPCR: quantitative polymerase chain reaction.

TABLE II Giardia duodenalis assemblages found in animals and in the environment in Brazilian states

State	Isolate origin	Assemblage
Amazonas	Human	A⁷²72. Nunes BC, Pavan MG, Jaeger LH, Monteiro KJ, Xavier SC, Monteiro FA, et al. Spatial and molecular epidemiology of Giardia intestinalis deep in the Amazon, Brazil. PLoS One. 2016; 11(7): e0158805.^,⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Amazonas	Human	B⁷²72. Nunes BC, Pavan MG, Jaeger LH, Monteiro KJ, Xavier SC, Monteiro FA, et al. Spatial and molecular epidemiology of Giardia intestinalis deep in the Amazon, Brazil. PLoS One. 2016; 11(7): e0158805.^,⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Ceará	Human	A⁶⁸68. Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008; 102(7): 718-25.^,⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Ceará	Human	B⁶⁸68. Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008; 102(7): 718-25.^,⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Piauí	Human	A⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Piauí	Human	B⁷⁶76. Nunes BC, Calegar DA, Pavan MG, Jaeger LH, Monteiro KJL, Dos Reis ERC, et al. Genetic diversity of Giardia duodenalis circulating in three Brazilian biomes. Infect Genet Evol. 2018; 59: 107-12.
Bahia	Human	A²¹21. Pacheco FTF, Carvalho SS, Cardoso LS, Andrade LS, das Chagas GMT, Gomes DC, et al. Immune response markers in sera of children infected with Giardia duodenalis AI and AII subassemblages. Immunobiology. 2019; 224(4): 595-603. B²¹21. Pacheco FTF, Carvalho SS, Cardoso LS, Andrade LS, das Chagas GMT, Gomes DC, et al. Immune response markers in sera of children infected with Giardia duodenalis AI and AII subassemblages. Immunobiology. 2019; 224(4): 595-603.
Minas Gerais	Human	A⁴⁶46. Gomes KB, Fernandes AP, Menezes A, Amorim Jr R, Silva EF, Rocha MO. Giardia duodenalis: genotypic comparison between a human and a canine isolates. Rev Soc Bras Med Trop. 2011; 44(4): 508-10.^,⁷⁴74. Scalia LA, Fava NM, Soares RM, Limongi JE, da Cunha MJ, Pena IF, et al. Multilocus genotyping of Giardia duodenalis in Brazilian children. Trans R Soc Trop Med Hyg. 2016; 110(6): 343-9.
		B⁷⁰70. Santos CK, Grama DF, Limongi JE, Costa FC, Couto TR, Soares RM, et al. Epidemiological, parasitological and molecular aspects of Giardia duodenalis infection in children attending public daycare centers in southeastern Brazil. Trans R Soc Trop Med Hyg. 2012; 106(8): 473-9.^,⁷⁴74. Scalia LA, Fava NM, Soares RM, Limongi JE, da Cunha MJ, Pena IF, et al. Multilocus genotyping of Giardia duodenalis in Brazilian children. Trans R Soc Trop Med Hyg. 2016; 110(6): 343-9.
		E⁷⁴74. Scalia LA, Fava NM, Soares RM, Limongi JE, da Cunha MJ, Pena IF, et al. Multilocus genotyping of Giardia duodenalis in Brazilian children. Trans R Soc Trop Med Hyg. 2016; 110(6): 343-9.
	Dog	A⁴⁶46. Gomes KB, Fernandes AP, Menezes A, Amorim Jr R, Silva EF, Rocha MO. Giardia duodenalis: genotypic comparison between a human and a canine isolates. Rev Soc Bras Med Trop. 2011; 44(4): 508-10.^,⁸⁴84. Fava NM, Soares RM, Scalia LA, Cunha MJ, Faria ES, Cury MC. Molecular typing of canine Giardia duodenalis isolates from Minas Gerais, Brazil. Exp Parasitol. 2016; 161: 1-5.
		B⁸⁴84. Fava NM, Soares RM, Scalia LA, Cunha MJ, Faria ES, Cury MC. Molecular typing of canine Giardia duodenalis isolates from Minas Gerais, Brazil. Exp Parasitol. 2016; 161: 1-5.
		C⁸⁴84. Fava NM, Soares RM, Scalia LA, Cunha MJ, Faria ES, Cury MC. Molecular typing of canine Giardia duodenalis isolates from Minas Gerais, Brazil. Exp Parasitol. 2016; 161: 1-5.
		D⁸⁴84. Fava NM, Soares RM, Scalia LA, Cunha MJ, Faria ES, Cury MC. Molecular typing of canine Giardia duodenalis isolates from Minas Gerais, Brazil. Exp Parasitol. 2016; 161: 1-5.
		E⁸⁴84. Fava NM, Soares RM, Scalia LA, Cunha MJ, Faria ES, Cury MC. Molecular typing of canine Giardia duodenalis isolates from Minas Gerais, Brazil. Exp Parasitol. 2016; 161: 1-5.
	Cattle	A⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
		B⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
		E⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
	Pig	E⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
	Sheep	B⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
	Sheep	E⁸⁶86. Fava NM, Soares RM, Scalia LA, Kalapothakis E, Pena IF, Vieira CU, et al. Performance of glutamate dehydrogenase and triose phosphate isomerase genes in the analysis of genotypic variability of isolates of Giardia duodenalis from livestocks. Biomed Res Int. 2013; 2013: 875048.
	Toco toucan	A³³33. da Cunha MJR, Cury MC, Santín M. Molecular identification of Enterocytozoon bieneusi, Cryptosporidium, and Giardia in Brazilian captive birds. Parasitol Res. 2017; 116(2): 487-93.
Rio de Janeiro	Human	A⁸8. Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis. 2016; 214(8): 1256-9.^,²⁸28. Volotão AC, Costa-Macedo LM, Haddad FS, Brandão A, Peralta JM, Fernandes O. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phylogenetic analysis. Acta Trop. 2007; 102(1): 10-9.^,⁴³43. Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MC. Molecular characterization of Giardia lamblia: first report of assemblage B in human isolates from Rio de Janeiro (Brazil). PLoS One. 2016; 11(8): e0160762.^,⁷⁵75. Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MDC. New multilocus genotypes of Giardia lamblia human isolates. Infect Genet Evol. 2017; 54: 128-37.
		B⁴³43. Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MC. Molecular characterization of Giardia lamblia: first report of assemblage B in human isolates from Rio de Janeiro (Brazil). PLoS One. 2016; 11(8): e0160762.^,⁷⁵75. Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MDC. New multilocus genotypes of Giardia lamblia human isolates. Infect Genet Evol. 2017; 54: 128-37.
		E⁸8. Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis. 2016; 214(8): 1256-9.
	Dog	A²⁸28. Volotão AC, Costa-Macedo LM, Haddad FS, Brandão A, Peralta JM, Fernandes O. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phylogenetic analysis. Acta Trop. 2007; 102(1): 10-9.^,⁸³83. Fantinatti M, Caseca AC, Bello AR, Fernandes O, Da-Cruz AM. The presence of Giardia lamblia assemblage A in dogs suggests an anthropozoonotic cycle of the parasite in Rio de Janeiro, Brazil. Infect Genet Evol. 2018; 65: 265-9.
	Cat	A²⁸28. Volotão AC, Costa-Macedo LM, Haddad FS, Brandão A, Peralta JM, Fernandes O. Genotyping of Giardia duodenalis from human and animal samples from Brazil using beta-giardin gene: a phylogenetic analysis. Acta Trop. 2007; 102(1): 10-9.
São Paulo	Human	A⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.^,⁶⁹69. Volotão AC, Ramos NM, Fantinatti M, Moraes MV, Netto HA, Storti-Melo LM, et al. Giardiasis as zoonosis: between proof of principle and paradigm in the Northwestern region of São Paulo State, Brazil. Braz J Infect Dis. 2011; 15(4): 382-3.^,⁷¹71. David ÉB, Guimarães S, de Oliveira AP, de Oliveira-Sequeira TCG, Bittencourt GN, Nardi ARM, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015; 8: 103.^,⁷³73. Oliveira-Arbex AP, David EB, Oliveira-Sequeira TC, Bittencourt GN, Guimarães S. Genotyping of Giardia duodenalis isolates in asymptomatic children attending daycare centre: evidence of high risk for anthroponotic transmission. Epidemiol Infect. 2016; 144(7): 1418-28.^,⁷⁸78. Corrêa CRT, Oliveira-Arbex AP, David ÉB, Guimarães S. Genetic analysis of Giardia duodenalis isolates from children of low-income families living in an economically successful region in southeastern Brazil. Rev Inst Med Trop São Paulo. 2020; 62: e20.
		B⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.^,⁷¹71. David ÉB, Guimarães S, de Oliveira AP, de Oliveira-Sequeira TCG, Bittencourt GN, Nardi ARM, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015; 8: 103.^,⁷³73. Oliveira-Arbex AP, David EB, Oliveira-Sequeira TC, Bittencourt GN, Guimarães S. Genotyping of Giardia duodenalis isolates in asymptomatic children attending daycare centre: evidence of high risk for anthroponotic transmission. Epidemiol Infect. 2016; 144(7): 1418-28.^,⁷⁸78. Corrêa CRT, Oliveira-Arbex AP, David ÉB, Guimarães S. Genetic analysis of Giardia duodenalis isolates from children of low-income families living in an economically successful region in southeastern Brazil. Rev Inst Med Trop São Paulo. 2020; 62: e20.
		C⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.
	Dog	A⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁹69. Volotão AC, Ramos NM, Fantinatti M, Moraes MV, Netto HA, Storti-Melo LM, et al. Giardiasis as zoonosis: between proof of principle and paradigm in the Northwestern region of São Paulo State, Brazil. Braz J Infect Dis. 2011; 15(4): 382-3.^,⁷¹71. David ÉB, Guimarães S, de Oliveira AP, de Oliveira-Sequeira TCG, Bittencourt GN, Nardi ARM, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015; 8: 103.
		B⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.
		C⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁴⁷47. Paz e Silva FM, Monobe MM, Lopes RS, Araujo Jr JP. Molecular characterization of Giardia duodenalis in dogs from Brazil. Parasitol Res. 2012; 110(1): 325-34.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.^,⁷¹71. David ÉB, Guimarães S, de Oliveira AP, de Oliveira-Sequeira TCG, Bittencourt GN, Nardi ARM, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015; 8: 103.
		D⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁴⁷47. Paz e Silva FM, Monobe MM, Lopes RS, Araujo Jr JP. Molecular characterization of Giardia duodenalis in dogs from Brazil. Parasitol Res. 2012; 110(1): 325-34.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.^,⁷¹71. David ÉB, Guimarães S, de Oliveira AP, de Oliveira-Sequeira TCG, Bittencourt GN, Nardi ARM, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015; 8: 103.
	Cat	A⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.
		B⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.
		D⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.
		F⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.
	Buffalo	E⁶⁰60. de Aquino MCC, Harvey TV, Inácio SV, Nagata WB, Ferrari ED, Oliveira BCM, et al. First description of Giardia duodenalis in buffalo calves (Bubalus bubalis) in southwest region of São Paulo State, Brazil. Food Waterborne Parasitol. 2019; 16: e00062.
	Cattle	A⁴⁰40. Paz e Silva FM, Lopes RS, Araújo Jr JP. Genetic characterisation of Giardia duodenalis in dairy cattle in Brazil. Folia Parasitol (Praha). 2012; 59(1): 15-20.^,⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.
	Cattle	E⁴⁰40. Paz e Silva FM, Lopes RS, Araújo Jr JP. Genetic characterisation of Giardia duodenalis in dairy cattle in Brazil. Folia Parasitol (Praha). 2012; 59(1): 15-20.^,⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁶⁷67. Souza SL, Gennari SM, Richtzenhain LJ, Pena HF, Funada MR, Cortez A, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007; 149(3-4): 258-64.
	Sheep	E⁵⁰50. Paz e Silva FM, Lopes RS, Bresciani KD, Amarante AF, Araujo Jr JP. High occurrence of Cryptosporidium ubiquitum and Giardia duodenalis genotype E in sheep from Brazil. Acta Parasitol. 2014; 59(1): 193-6.
	Nonhuman primates	A⁸⁵85. David ÉB, Patti M, Coradi ST, Oliveira-Sequeira TC, Ribolla PE, Guimarães S. Molecular typing of Giardia duodenalis isolates from nonhuman primates housed in a Brazilian zoo. Rev Inst Med Trop São Paulo. 2014; 56(1): 49-54.
	Oyster	A⁵⁸58. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M, et al. Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res. 2018; 137: 273-80.
	Water and/or Sewage	A⁴⁴44. Ulloa-Stanojlovic FM, Aguiar B, Jara LM, Sato MI, Guerrero JA, Hachich E, et al. Occurrence of Giardia intestinalis and Cryptosporidium sp. in wastewater samples from São Paulo State, Brazil, and Lima, Peru. Environ Sci Pollut Res Int. 2016; 23(21): 22197-205.^,⁴⁵45. de Araújo RS, Aguiar B, Dropa M, Razzolini MTP, Sato MIZ, Lauretto MS, et al. Detection and molecular characterization of Cryptosporidium species and Giardia assemblages in two watersheds in the metropolitan region of São Paulo, Brazil. Environ Sci Pollut Res Int. 2018; 25(15): 15191-203.^,⁵⁷57. Fernandes LN, de Souza PP, de Araújo RS, Razzolini MT, Soares RM, Sato MI, et al. Detection of assemblages A and B of Giardia duodenalis in water and sewage from São Paulo State, Brazil. J Water Health. 2011; 9(2): 361-7.^,⁵⁸58. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M, et al. Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res. 2018; 137: 273-80.^,⁵⁹59. Yamashiro S, Foco MLR, Pineda CO, José J, Nour EAA, Siqueira-Castro ICV, et al. Giardia spp. and Cryptosporidium spp. removal efficiency of a combined fixed-film system treating domestic wastewater receiving hospital effluent. Environ Sci Pollut Res Int. 2019; 26(22): 22756-71.^,⁶¹61. Pineda CO, Leal DAG, Fiuza VRDS, Jose J, Borelli G, Durigan M, et al. Toxoplasma gondii oocysts, Giardia cysts and Cryptosporidium oocysts in outdoor swimming pools in Brazil. Zoonoses Public Health. 2020; 67(7): 785-95.
		B⁵⁷57. Fernandes LN, de Souza PP, de Araújo RS, Razzolini MT, Soares RM, Sato MI, et al. Detection of assemblages A and B of Giardia duodenalis in water and sewage from São Paulo State, Brazil. J Water Health. 2011; 9(2): 361-7.^,⁵⁹59. Yamashiro S, Foco MLR, Pineda CO, José J, Nour EAA, Siqueira-Castro ICV, et al. Giardia spp. and Cryptosporidium spp. removal efficiency of a combined fixed-film system treating domestic wastewater receiving hospital effluent. Environ Sci Pollut Res Int. 2019; 26(22): 22756-71.^,⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.^,⁴⁴44. Ulloa-Stanojlovic FM, Aguiar B, Jara LM, Sato MI, Guerrero JA, Hachich E, et al. Occurrence of Giardia intestinalis and Cryptosporidium sp. in wastewater samples from São Paulo State, Brazil, and Lima, Peru. Environ Sci Pollut Res Int. 2016; 23(21): 22197-205.
		C⁵⁸58. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M, et al. Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res. 2018; 137: 273-80.^,⁵⁹59. Yamashiro S, Foco MLR, Pineda CO, José J, Nour EAA, Siqueira-Castro ICV, et al. Giardia spp. and Cryptosporidium spp. removal efficiency of a combined fixed-film system treating domestic wastewater receiving hospital effluent. Environ Sci Pollut Res Int. 2019; 26(22): 22756-71.
		D⁴²42. Durigan M, Abreu AG, Zucchi MI, Franco RM, de Souza AP. Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One. 2014; 9(12): e115489.
Paraná	Human	A⁴⁸48. Colli CM, Bezagio RC, Nishi L, Ferreira ÉC, Falavigna-Guilherme AL, Gomes ML. Food handlers as a link in the chain of transmission of Giardia duodenalis and other protozoa in public schools in southern Brazil. Trans R Soc Trop Med Hyg. 2015; 109(9): 601-3.^,⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.^,⁷⁷77. Seguí R, Muñoz-Antoli C, Klisiowicz DR, Oishi CY, Köster PC, de Lucio A, et al. Prevalence of intestinal parasites, with emphasis on the molecular epidemiology of Giardia duodenalis and Blastocystis sp., in the Paranaguá Bay, Brazil: a community survey. Parasit Vectors. 2018; 11(1): 490.
	Human	B⁴⁸48. Colli CM, Bezagio RC, Nishi L, Ferreira ÉC, Falavigna-Guilherme AL, Gomes ML. Food handlers as a link in the chain of transmission of Giardia duodenalis and other protozoa in public schools in southern Brazil. Trans R Soc Trop Med Hyg. 2015; 109(9): 601-3.^,⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.^,⁷⁷77. Seguí R, Muñoz-Antoli C, Klisiowicz DR, Oishi CY, Köster PC, de Lucio A, et al. Prevalence of intestinal parasites, with emphasis on the molecular epidemiology of Giardia duodenalis and Blastocystis sp., in the Paranaguá Bay, Brazil: a community survey. Parasit Vectors. 2018; 11(1): 490.
	Dog	B⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.
		C⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.
		D⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.
	Vegetable	A⁵¹51. Rafael K, Marchioro AA, Colli CM, Tiyo BT, Evangelista FF, Bezagio RC, et al. Genotyping of Giardia duodenalis in vegetables cultivated with organic and chemical fertilizer from street markets and community vegetable gardens in a region of Southern Brazil. Trans R Soc Trop Med Hyg. 2017; 111(12): 540-5.^,⁶²62. Tiyo R, de Souza CZ, Piovesani AFA, Tiyo BT, Colli CM, Marchioro AA, et al. Predominance of Giardia duodenalis assemblage AII in fresh leafy vegetables from a market in southern Brazil. J Food Prot. 2016; 79(6): 1036-9.
		B⁴⁹49. Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS One. 2015; 10(3): e0118065.^,⁵¹51. Rafael K, Marchioro AA, Colli CM, Tiyo BT, Evangelista FF, Bezagio RC, et al. Genotyping of Giardia duodenalis in vegetables cultivated with organic and chemical fertilizer from street markets and community vegetable gardens in a region of Southern Brazil. Trans R Soc Trop Med Hyg. 2017; 111(12): 540-5.
		E⁴¹41. Ferreira FP, Caldart ET, Freire RL, Mitsuka-Breganó R, Freitas FM, Miura AC, et al. The effect of water source and soil supplementation on parasite contamination in organic vegetable gardens. Rev Bras Parasitol Vet. 2018; 27(3): 327-37.^,⁵¹51. Rafael K, Marchioro AA, Colli CM, Tiyo BT, Evangelista FF, Bezagio RC, et al. Genotyping of Giardia duodenalis in vegetables cultivated with organic and chemical fertilizer from street markets and community vegetable gardens in a region of Southern Brazil. Trans R Soc Trop Med Hyg. 2017; 111(12): 540-5.
	Water	E⁴¹41. Ferreira FP, Caldart ET, Freire RL, Mitsuka-Breganó R, Freitas FM, Miura AC, et al. The effect of water source and soil supplementation on parasite contamination in organic vegetable gardens. Rev Bras Parasitol Vet. 2018; 27(3): 327-37.
	Soil	E⁴¹41. Ferreira FP, Caldart ET, Freire RL, Mitsuka-Breganó R, Freitas FM, Miura AC, et al. The effect of water source and soil supplementation on parasite contamination in organic vegetable gardens. Rev Bras Parasitol Vet. 2018; 27(3): 327-37.
Santa Catarina	Human	A⁵²52. Quadros RM, Weiss PH, Marques SM, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop São Paulo. 2016; 58: 66.
	Human	B⁵²52. Quadros RM, Weiss PH, Marques SM, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop São Paulo. 2016; 58: 66.
	Dog	A⁵²52. Quadros RM, Weiss PH, Marques SM, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop São Paulo. 2016; 58: 66.
		B⁵²52. Quadros RM, Weiss PH, Marques SM, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop São Paulo. 2016; 58: 66.
		C⁵²52. Quadros RM, Weiss PH, Marques SM, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop São Paulo. 2016; 58: 66.
	Nonhuman primates	A³¹31. Volotão AC, Júnior JC, Grassini C, Peralta JM, Fernandes O. Genotyping of Giardia duodenalis from southern brown howler monkeys (Alouatta clamitans) from Brazil. Vet Parasitol. 2008; 158(1-2): 133-7.
Uninformed	Jaguar	A³²32. Soares RM, de Souza SL, Silveira LH, Funada MR, Richtzenhain LJ, Gennari SM. Genotyping of potentially zoonotic Giardia duodenalis from exotic and wild animals kept in captivity in Brazil. Vet Parasitol. 2011; 180(3-4): 344-8.
	Monkey	B³²32. Soares RM, de Souza SL, Silveira LH, Funada MR, Richtzenhain LJ, Gennari SM. Genotyping of potentially zoonotic Giardia duodenalis from exotic and wild animals kept in captivity in Brazil. Vet Parasitol. 2011; 180(3-4): 344-8.
	Chinchilla	B³²32. Soares RM, de Souza SL, Silveira LH, Funada MR, Richtzenhain LJ, Gennari SM. Genotyping of potentially zoonotic Giardia duodenalis from exotic and wild animals kept in captivity in Brazil. Vet Parasitol. 2011; 180(3-4): 344-8.
	Ostriches	B³²32. Soares RM, de Souza SL, Silveira LH, Funada MR, Richtzenhain LJ, Gennari SM. Genotyping of potentially zoonotic Giardia duodenalis from exotic and wild animals kept in captivity in Brazil. Vet Parasitol. 2011; 180(3-4): 344-8.

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Epidemiology of <i>Giardia duodenalis</i> assemblages in Brazil: there is still a long way to go

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[1] + Corresponding author: fantinatti@ioc.fiocruz.br