Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities

Abstract Background There are close similarities between the life-cycles of Echinococcus granulosus sensu lato (E. granulosus s.l.) that causes cystic echinococcosis (CE) in humans and Taenia multiceps/Coenurus cerebralis that causes cerebral coenurosis in small ruminants. Recent evidence highlights...

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Main Authors: Francesca Tamarozzi, Tito Kibona, William A. de Glanville, Tauta Mappi, Elly Adonikamu, Anande Salewi, Kennedy Misso, Venance Maro, Adriano Casulli, Azzurra Santoro, Federica Santolamazza, Blandina T. Mmbaga, Sarah Cleaveland
Format: Article
Language:English
Published: BMC 2022-10-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-022-05518-x
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author Francesca Tamarozzi
Tito Kibona
William A. de Glanville
Tauta Mappi
Elly Adonikamu
Anande Salewi
Kennedy Misso
Venance Maro
Adriano Casulli
Azzurra Santoro
Federica Santolamazza
Blandina T. Mmbaga
Sarah Cleaveland
author_facet Francesca Tamarozzi
Tito Kibona
William A. de Glanville
Tauta Mappi
Elly Adonikamu
Anande Salewi
Kennedy Misso
Venance Maro
Adriano Casulli
Azzurra Santoro
Federica Santolamazza
Blandina T. Mmbaga
Sarah Cleaveland
author_sort Francesca Tamarozzi
collection DOAJ
description Abstract Background There are close similarities between the life-cycles of Echinococcus granulosus sensu lato (E. granulosus s.l.) that causes cystic echinococcosis (CE) in humans and Taenia multiceps/Coenurus cerebralis that causes cerebral coenurosis in small ruminants. Recent evidence highlights that livestock in Maasai communities of northern Tanzania are suffering from increases in the prevalence of cerebral coenurosis, leading to concerns about a possible concurrent increased risk of human CE. The aim of this study was to estimate the prevalence of human abdominal CE and the prevalence and species/genotypes of E. granulosus s.l. in livestock in Maasai communities. Methods Human CE was diagnosed by abdominal ultrasound on volunteers aged ≥ 7 years in five villages in the Longido and Ngorongoro Districts in northern Tanzania. Infection in ruminants was evaluated through inspection in local abattoirs, followed by molecular identification of one cyst per animal, with a priority for hepatic cysts, using PCR targeting of the cytochrome c oxidase I gene (COX1), followed by restriction fragment length polymorphism and multiplex PCR, and sequencing of non-E. granulosus s.l. samples. Results Ultrasound was performed on 823 volunteers (n = 352 in two villages in Longido District, and n = 471 in three villages of Ngorongoro). Hepatic CE cases were diagnosed only in Ngorongoro (n = 6; 1.3%), of which three had active cysts. Village-level prevalence of CE ranged between 0 and 2.4%. Of the 697 ruminants inspected, 34.4% had parasitic cysts. Molecular identification was achieved for 140 of the 219 (63.9%) cysts sampled. E. granulosus s.l. and T. hydatigena/Cysticercus tenuicollis were identified in 51.4% and 48.6%, respectively, of livestock cysts. E. granulosus s.l. was identified in livestock from both Longido (35.3% of 116 genotyped cysts) and Ngorongoro (91.2% of 34 genotyped cysts). Of the total of 72 E. granuslosus s.l. cysts identified in livestock, 87.5% were E. granulosus sensu strict o (G1–G3 genotypes), 9.7% were E. ortleppi (G5) and one cyst was E. canadensis (G6–10). The three active human cysts, which were removed surgically, were G1–G3 genotypes. Conclusions Multiple species/genotypes of E. granulosus s.l. are circulating in Maasai communities of northern Tanzania. Human CE was detected in villages of Ngorongoro District and a high prevalence of echinococcal cysts was observed in livestock in both districts. More precise estimation of the prevalence in this area and a better understanding of the specific risk factors for CE among Maasai communities in northern Tanzania is needed. Interventions targeting transmission routes common to both E. granulosus s.l. and T. multiceps would have dual benefits for preventing both human and livestock disease. Graphical Abstract
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spelling doaj.art-bb3aabd62deb41d69407ac3457cabc702022-12-22T04:34:43ZengBMCParasites & Vectors1756-33052022-10-0115111110.1186/s13071-022-05518-xCystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communitiesFrancesca Tamarozzi0Tito Kibona1William A. de Glanville2Tauta Mappi3Elly Adonikamu4Anande Salewi5Kennedy Misso6Venance Maro7Adriano Casulli8Azzurra Santoro9Federica Santolamazza10Blandina T. Mmbaga11Sarah Cleaveland12IRCCS Sacro Cuore Don Calabria HospitalKilimanjaro Clinical Research InstituteUniversity of GlasgowKilimanjaro Clinical Research InstituteKilimanjaro Christian Medical CentreKilimanjaro Christian Medical CentreKilimanjaro Christian Medical CentreKilimanjaro Christian Medical CentreIstituto Superiore di SanitàIstituto Superiore di SanitàIstituto Superiore di SanitàKilimanjaro Christian Medical CentreUniversity of GlasgowAbstract Background There are close similarities between the life-cycles of Echinococcus granulosus sensu lato (E. granulosus s.l.) that causes cystic echinococcosis (CE) in humans and Taenia multiceps/Coenurus cerebralis that causes cerebral coenurosis in small ruminants. Recent evidence highlights that livestock in Maasai communities of northern Tanzania are suffering from increases in the prevalence of cerebral coenurosis, leading to concerns about a possible concurrent increased risk of human CE. The aim of this study was to estimate the prevalence of human abdominal CE and the prevalence and species/genotypes of E. granulosus s.l. in livestock in Maasai communities. Methods Human CE was diagnosed by abdominal ultrasound on volunteers aged ≥ 7 years in five villages in the Longido and Ngorongoro Districts in northern Tanzania. Infection in ruminants was evaluated through inspection in local abattoirs, followed by molecular identification of one cyst per animal, with a priority for hepatic cysts, using PCR targeting of the cytochrome c oxidase I gene (COX1), followed by restriction fragment length polymorphism and multiplex PCR, and sequencing of non-E. granulosus s.l. samples. Results Ultrasound was performed on 823 volunteers (n = 352 in two villages in Longido District, and n = 471 in three villages of Ngorongoro). Hepatic CE cases were diagnosed only in Ngorongoro (n = 6; 1.3%), of which three had active cysts. Village-level prevalence of CE ranged between 0 and 2.4%. Of the 697 ruminants inspected, 34.4% had parasitic cysts. Molecular identification was achieved for 140 of the 219 (63.9%) cysts sampled. E. granulosus s.l. and T. hydatigena/Cysticercus tenuicollis were identified in 51.4% and 48.6%, respectively, of livestock cysts. E. granulosus s.l. was identified in livestock from both Longido (35.3% of 116 genotyped cysts) and Ngorongoro (91.2% of 34 genotyped cysts). Of the total of 72 E. granuslosus s.l. cysts identified in livestock, 87.5% were E. granulosus sensu strict o (G1–G3 genotypes), 9.7% were E. ortleppi (G5) and one cyst was E. canadensis (G6–10). The three active human cysts, which were removed surgically, were G1–G3 genotypes. Conclusions Multiple species/genotypes of E. granulosus s.l. are circulating in Maasai communities of northern Tanzania. Human CE was detected in villages of Ngorongoro District and a high prevalence of echinococcal cysts was observed in livestock in both districts. More precise estimation of the prevalence in this area and a better understanding of the specific risk factors for CE among Maasai communities in northern Tanzania is needed. Interventions targeting transmission routes common to both E. granulosus s.l. and T. multiceps would have dual benefits for preventing both human and livestock disease. Graphical Abstracthttps://doi.org/10.1186/s13071-022-05518-xEchinococcus granulosus sensu latoCystic echinococcosisMaasaiNorthern TanzaniaPrevalenceGenotypes
spellingShingle Francesca Tamarozzi
Tito Kibona
William A. de Glanville
Tauta Mappi
Elly Adonikamu
Anande Salewi
Kennedy Misso
Venance Maro
Adriano Casulli
Azzurra Santoro
Federica Santolamazza
Blandina T. Mmbaga
Sarah Cleaveland
Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
Parasites & Vectors
Echinococcus granulosus sensu lato
Cystic echinococcosis
Maasai
Northern Tanzania
Prevalence
Genotypes
title Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
title_full Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
title_fullStr Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
title_full_unstemmed Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
title_short Cystic echinococcosis in northern Tanzania: a pilot study in Maasai livestock-keeping communities
title_sort cystic echinococcosis in northern tanzania a pilot study in maasai livestock keeping communities
topic Echinococcus granulosus sensu lato
Cystic echinococcosis
Maasai
Northern Tanzania
Prevalence
Genotypes
url https://doi.org/10.1186/s13071-022-05518-x
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