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Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin

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A special issue of Tropical Medicine and Infectious Disease (ISSN 2414-6366). This special issue belongs to the section "Infectious Diseases".

Deadline for manuscript submissions: closed (15 December 2022) | Viewed by 35254

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Prof. Dr. Eli Schwartz

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Guest Editor

1. Director of the Institute of Geographic Medicine & Tropical Diseases, Chaim Sheba Medical Center, Tel Hashomer 52621, Israel
2. Professor of Medicine, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Interests: clinical tropical medicine; malaria; schistosomiasis; typhoid fever; arboviruses; travel medicine

Prof. Dr. Michael Libman

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Guest Editor

Department of Medicine, Division of Infectious Diseases, Faculty of Medicine, McGill University, Montreal, QC H3A 0G4, Canada
Interests: tropical diseases; parasitology; travel medicine; epidemiology; infectious diseases

Special Issue Information

Dear Colleagues,

Schistosomiasis is one of the most common, but still neglected, infectious diseases prevalent in many tropical countries. Due to increase travel and migration, it is seen with increasing frequency in non-endemic areas around the world. Despite the passage of over 150 years since the description of the pathogen causing the disease, there are still deficiencies in terms of sensitive and specific diagnostic tests, efficient treatments for both acute and chronic infection, tests of cure, and programs for control and prevention, both in endemic areas and in traveler populations.

In this Special Issue we will try to summarize the existing data, current research, and the lacunae in our knowledge of the clinical spectrum, disease evolution, diagnostic methods, treatment modalities and indication, and prevention for this parasitic infection. In many cases, consideration of both the questions and the answers will differ when examining the situation in endemic regions as compared to traveler- and migration-associated infection. We hope this Issue will help to provide guidance to providers of health care, both to residents of endemic areas and for those travelling to and from regions of transmission risk.

Prof. Dr. Eli Schwartz
Prof. Dr. Michael Libman
Guest Editors

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Keywords

• Schistosoma
• Schistosomiasis
• S. mansoni
• S. hematobium
• S. japonicum
• Travelers
• Immigrants
• Endemic region
• Control
• Prevention
• Vaccine

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Published Papers (10 papers)

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12 pages, 866 KiB

Open AccessArticle

Natural History of Hepatosplenic Schistosomiasis (HSS) Non–Cirrhotic Portal Hypertension (NCPH): Influence of Gastrointestinal Bleeding and Decompensation in Prognosis

by Zulane S. T. Veiga, Flávia F. Fernandes, Lívia Guimarães, Juliana Piedade and Gustavo Henrique S. Pereira

Trop. Med. Infect. Dis. 2023, 8(3), 145; https://doi.org/10.3390/tropicalmed8030145 - 27 Feb 2023

Cited by 3 | Viewed by 2961

Abstract

Background: Hepatosplenic schistosomiasis (HSS) is a peculiar form of non-cirrhotic portal hypertension (NCPH). Although HSS patients present normal hepatic function, some evolve signs of hepatocellular failure and features of decompensated cirrhosis. The natural history of HSS-NCPH is unknown. Methods: A retrospective study was conducted that evaluated patients who fulfilled clinical-laboratorial criteria for HSS. Results: A total of 105 patients were included. Eleven patients already presented with decompensated disease and had lower transplant-free survival at 5 years than those without (61% vs. 95%, p = 0.015). Among 94 patients without prior decompensation, the median follow-up was 62 months and 44% of them had varicose bleeding (two or more episodes in 27%). Twenty-one patients presented at least one episode of decompensation (10-year probability 38%). Upon multivariate analysis, varicose bleeding and higher bilirubin levels were associated with decompensation. The 10-year probability of survival was 87%. Development of decompensation and age were predictive of mortality. Conclusion: HSS is characterized by multiple episodes of GI bleeding, a high probability of decompensation and reduced survival at the end of the first decade. Decompensation is more common in patients with varicose esophageal bleeding and is associated with lower survival. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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20 pages, 2855 KiB

Open AccessArticle

Geographical Influence on Morphometric Variability of Genetically “Pure” Schistosoma haematobium Eggs from Sub-Saharan Migrants in Spain

by Marta Reguera-Gómez, Maria Adela Valero, Patricio Artigas, Alejandra De Elías-Escribano, Maria Cecilia Fantozzi, Maria Pilar Luzón-García, Joaquín Salas-Coronas, Jérôme Boissier, Santiago Mas-Coma and Maria Dolores Bargues

Trop. Med. Infect. Dis. 2023, 8(3), 144; https://doi.org/10.3390/tropicalmed8030144 - 27 Feb 2023

Cited by 2 | Viewed by 5911

Abstract

Schistosome eggs play a key role in schistosomiasis diagnosis and research. The aim of this work is to morphogenetically study the eggs of Schistosoma haematobium found in sub-Saharan migrants present in Spain, analyzing their morphometric variation in relation to the geographical origin of the parasite (Mali, Mauritania and Senegal). Only eggs considered “pure” S. haematobium by genetic characterization (rDNA ITS-2 and mtDNA cox1) have been used. A total of 162 eggs obtained from 20 migrants from Mali, Mauritania and Senegal were included in the study. Analyses were made by the Computer Image Analysis System (CIAS). Following a previously standardized methodology, seventeen measurements were carried out on each egg. The morphometric analysis of the three morphotypes detected (round, elongated and spindle) and the biometric variations in relation to the country of origin of the parasite on the egg phenotype were carried out by canonical variate analysis. Mahalanobis distances, when all egg measurements were analyzed, showed differences between: (i) Mali-Mauritania, Mali-Senegal and Mauritania-Senegal in the round morphotype; (ii) Mali-Mauritania and Mauritania-Senegal in the elongated morphotype; and (iii) Mauritania-Senegal in the spindle morphotype. Mahalanobis distances, when spine variables were analyzed, showed differences between Mali-Senegal in the round morphotype. In conclusion, this is the first phenotypic study performed on individually genotyped “pure” S. haematobium eggs, allowing the assessment of the intraspecific morphological variations associated with the geographical origin of the schistosome eggs. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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11 pages, 2135 KiB

Open AccessCommunication

Biomphalaria pfeifferi (Gastropoda: Planorbidae) in Lake Malawi and Upper Shire River, Mangochi District, Malawi: Distribution, Genetic Diversity and Pre-Patent Schistosome Infections

by Mohammad H. Alharbi, Charlotte Condemine, Josie Hesketh, Sekeleghe A. Kayuni, Thomas M. Arme, John Archer, Sam Jones, E. James LaCourse, Peter Makaula, Janelisa Musaya and J. Russell Stothard

Trop. Med. Infect. Dis. 2023, 8(2), 126; https://doi.org/10.3390/tropicalmed8020126 - 18 Feb 2023

Cited by 6 | Viewed by 2678

Abstract

In November 2017, Biomphalaria pfeifferi, the key intermediate host for Schistosoma mansoni in Africa, was first reported in Lake Malawi, Mangochi District. Two subsequent malacological surveys in 2018 and 2019 confirmed its lacustrine presence, as well as its presence along the Upper Shire River. These surveys provided sufficient specimens for analyses of the genetic structure and a transmission assessment for intestinal schistosomiasis. A total of 76 collected snails were characterized by a DNA sequence analysis of a 650 bp fragment of the mitochondrial cytochrome oxidase subunit 1 (cox1); by size fractionation of six fluorescently labelled microsatellite loci (Bgμl16, Bgμl, Bpf8, rg6, U-7, and rg9);by denaturing PAGE; and by detection of pre-patent Schistosoma infection by real-time PCR with a TaqMan^® probe. Five closely related cox1 haplotypes were identified, all present within a single location, with only one haplotype common across all the other locations sampled. No allelic size variation was detected with the microsatellites and all loci were monomorphic. Overall, the pre-patent prevalence of Schistosoma spp. was 31%, with infected snails found at several sampling locations. In this part of Lake Malawi, Bi. pfeifferi exhibits low genetic diversity and is clearly being exposed to the miracidia of S. mansoni, which is likely facilitating the autochthonous transmission of this parasite. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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13 pages, 1703 KiB

Open AccessArticle

Evaluation of Two Different Strategies for Schistosomiasis Screening in High-Risk Groups in a Non-Endemic Setting

by Luisa Roade, Elena Sulleiro, Cristina Bocanegra, Fernando Salvador, Begoña Treviño, Francesc Zarzuela, Lidia Goterris, Nuria Serre-Delcor, Inés Oliveira-Souto, Maria Luisa Aznar, Diana Pou, Adrián Sánchez-Montalvà, Pau Bosch-Nicolau, Juan Espinosa-Pereiro and Israel Molina

Trop. Med. Infect. Dis. 2023, 8(1), 44; https://doi.org/10.3390/tropicalmed8010044 - 6 Jan 2023

Cited by 1 | Viewed by 2578

Abstract

A consensus on the recommended screening algorithms for schistosomiasis in asymptomatic high-risk subjects in non-endemic areas is lacking. The objective of this study was to evaluate the real-life performance of direct microscopy and ELISA serology for schistosomiasis screening in a high-risk population in a non-endemic setting. A retrospective cohort study was conducted in two out-patient Tropical Medicine units in Barcelona (Spain) from 2014 to 2017. Asymptomatic adults arriving from the Sub-Saharan region were included. Schistosomiasis screening was conducted according to clinical practice following a different strategy in each setting: (A) feces and urine direct examination plus S. mansoni serology if non-explained eosinophilia was present and (B) S. mansoni serology plus uroparasitological examination as the second step in case of a positive serology. Demographic, clinical and laboratory features were collected. Schistosomiasis cases, clinical management and a 24 month follow-up were recorded for each group. Four-hundred forty individuals were included. The patients were mainly from West African countries. Fifty schistosomiasis cases were detected (11.5% group A vs. 4 % group B, p = 0.733). When both microscopic and serological techniques were performed, discordant results were recorded in 18.4% (16/88). Schistosomiasis cases were younger (p < 0.001) and presented eosinophilia and elevated IgE (p < 0.001) more frequently. Schistosomiasis is a frequent diagnosis among high-risk populations. Serology achieves a similar performance to direct diagnosis for the screening of schistosomiasis in a high-risk population. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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11 pages, 1412 KiB

Open AccessArticle

Diagnosis of Schistosomiasis without a Microscope: Evaluating Circulating Antigen (CCA, CAA) and DNA Detection Methods on Banked Samples of a Community-Based Survey from DR Congo

by Pytsje T. Hoekstra, Joule Madinga, Pascal Lutumba, Rebecca van Grootveld, Eric A. T. Brienen, Paul L. A. M. Corstjens, Govert J. van Dam, Katja Polman and Lisette van Lieshout

Trop. Med. Infect. Dis. 2022, 7(10), 315; https://doi.org/10.3390/tropicalmed7100315 - 19 Oct 2022

Cited by 12 | Viewed by 2992

Abstract

Detection of Schistosoma eggs in stool or urine is known for its low sensitivity in diagnosing light infections. Alternative diagnostics with better sensitivity while remaining highly specific, such as real-time PCR and circulating antigen detection, are progressively used as complementary diagnostic procedures but have not yet replaced microscopy. This study evaluates these alternative methods for the detection of Schistosoma infections in the absence of microscopy. Schistosomiasis presence was determined retrospectively in 314 banked stool and urine samples, available from a previous survey on the prevalence of taeniasis in a community in the Democratic Republic of the Congo, using real-time PCR, the point-of-care circulating cathodic antigen (POC-CCA) test, as well as the up-converting particle lateral flow circulating anodic antigen (UCP-LF CAA) test. Schistosoma DNA was present in urine (3%) and stool (28%) samples, while CCA (28%) and CAA (69%) were detected in urine. Further analysis of the generated data indicated stool-based PCR and the POC-CCA test to be suitable diagnostics for screening of S. mansoni infections, even in the absence of microscopy. A substantial proportion (60%) of the 215 CAA-positive cases showed low antigen concentrations, suggesting that even PCR and POC-CCA underestimated the “true” number of schistosome positives. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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8 pages, 245 KiB

Open AccessArticle

Schistosomiasis Control in Ethiopia: The Role of Snail Mapping in Endemic Communities

by Asrat Meleko, Sarah Li, Dorin Brener Turgeman, Michal Bruck, Nisan Z. Kesete, Willemijn Zaadnoordijk, David Rollinson, Galia Sabar, Zvi Bentwich and Rachel Golan

Trop. Med. Infect. Dis. 2022, 7(10), 272; https://doi.org/10.3390/tropicalmed7100272 - 28 Sep 2022

Cited by 4 | Viewed by 3054

Abstract

Introduction: Schistosomiasis, a neglected tropical disease (NTD), remains a public health problem in Ethiopia. Freshwater snails, acting as intermediate hosts, release cercariae, the infectious parasite, into the water, which penetrate human skin that encounters infested waters. The objective of this study was to map snail abundance along rivers and study its association with schistosomiasis infection in communities using these rivers. Materials and Methods: A cross-sectional study was carried out at 20 river sites in Mizan Aman city administration, Bench Sheko zone, South West Ethiopia Peoples (SWEP) region, Ethiopia, to study the distribution of host snails and transmission sites for intestinal schistosomiasis. This study used a quantitative database consisting of data on the prevalence of infected snails, the characteristics of rivers and riverbanks, and the prevalence of schistosomiasis in the community, based on stool samples collected from community members near the sampling sites. Results: Aquatic snails were found in 11 of the 20 sites sampled. A total of 598 snails was collected, including Biomphalaria pfeifferi, Biomphalaria sudanica, Radix natalensis and Bulinus globosus species; the most abundant species was Biomphalaria pfeifferi. Stool samples were collected from 206 community members from all 20 sites. Forty-one (19.9%) were positive for Schistosoma mansoni. A positive correlation was found between the presence of snails and positive stool samples (r = 0.60, p = 0.05) and between the presence of infected snails and the prevalence of infection (r = 0.64, p = 0.03). Locations with muddy riverbanks were associated with the presence of snails (r = 0.81, p < 0.001). Conclusions: These results emphasize the importance of mapping snails for the control of schistosomiasis by defining hotspots of infection and identifying factors associated with the presence of infected snails. The results support the need for a continuous mapping of snails and the introduction of snail control as a major element for the successful control of schistosomiasis in endemic communities. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

14 pages, 1696 KiB

Open AccessArticle

Prevalence and Molecular Identification of Schistosoma haematobium among Children in Lusaka and Siavonga Districts, Zambia

by Rabecca Tembo, Walter Muleya, John Yabe, Henson Kainga, King S. Nalubamba, Mildred Zulu, Florence Mwaba, Shereen Ahmed Saad, Moses Kamwela, Andrew N. Mukubesa, Ngula Monde, Simegnew Adugna Kallu, Natalia Mbewe and Andrew M. Phiri

Trop. Med. Infect. Dis. 2022, 7(9), 239; https://doi.org/10.3390/tropicalmed7090239 - 10 Sep 2022

Cited by 3 | Viewed by 3667

Abstract

Schistosomiasis remains a public health concern in Zambia. Urinary schistosomiasis caused by Schistosoma haematobium is the most widely distributed infection. The aim of the current study was to determine the prevalence and risk factors of urinary schistosomiasis and identify the strain of S. haematobium among children in the Siavonga and Lusaka districts in Zambia. Urine samples were collected from 421 primary school children and S. haematobium eggs were examined under light microscopy. A semi-structured questionnaire was used to obtain information on the socio-demographic characteristics and the potential risk factors for urinary schistosomiasis. DNA of the parasite eggs was extracted from urine samples and the internal transcribed spacer gene was amplified, sequenced and phylogenetically analysed. The overall prevalence of S. haematobium was 9.7% (41/421) (95% CI: 7.16–13.08), male participants made up 6.2% (26/232) (95% CI: 4.15–9.03), having a higher burden of disease than female participants who made up 3.5% (15/421) (95% CI: 2.01–5.94). The age group of 11–15 years had the highest overall prevalence of 8.3% (35/421) (5.94–11.48). Participants that did not go fishing were 0.008 times less likely to be positive for schistosomiasis while participants whose urine was blood-tinged or cloudy on physical examination and those that lived close to water bodies were 9.98 and 11.66 times more likely to test positive for schistosomiasis, respectively. A phylogenetic tree analysis indicated that S. haematobium isolates were closely related to pure S. haematobium from Zimbabwe and hybrids of S. haematobium × S. bovis from Benin, Senegal and Malawi. The current study shows that urinary schistosomiasis is endemic in the study areas and is associated with water contact, and S. haematobium isolated is closely related to hybrids of S. bovis × S. haematobium strain, indicating the zoonotic potential of this parasite. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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8 pages, 446 KiB

Open AccessArticle

Sustainable Elimination of Schistosomiasis in Ethiopia—A Five-Year Follow-Up Study

by Lotte Ben Gal, Michal Bruck, Robyn Tal, Sarit Baum, Jemal Mahdi Ali, Lemlem Legesse Weldegabriel, Galia Sabar, Rachel Golan and Zvi Bentwich

Trop. Med. Infect. Dis. 2022, 7(9), 218; https://doi.org/10.3390/tropicalmed7090218 - 1 Sep 2022

Cited by 2 | Viewed by 2674

Abstract

In 2009, Mekele, the capital of the Tigray Region in Ethiopia, presented a mean prevalence of 44.7% of schistosomiasis (S. mansoni) in school children. Termed a public health problem, NALA, an international public health non-governmental organization, and their partners implemented a novel model of intervention, which aimed to compliment mass drug administration (MDA) campaigns with behavioral change (BC) and improved sanitation to achieve sustained elimination of schistosomiasis. The four-year intervention (2009–2012) covered 38 primary schools. The objective of this study was to examine factors associated with control or resurgence of the disease, and the association between the behavioral change program and disease prevalence, ten years after initiation. Eleven primary schools were selected for this follow-up study. All students provided a stool sample and filled in a knowledge, attitude and practice (KAP) questionnaire. In seven out of eleven schools (63.6%) the prevalence of schistosomiasis was maintained below 2% ten years after the initiation of the intervention. In four schools, prevalence returned to pre-intervention levels, defining them as persistent hot spots (PHS). Students from PHS schools scored lower on KAP questionnaires compared to students from responder schools; 3.9 ± 0.9 vs. 4.2 ± 0.9 (p-value < 0.001) for practice questions and 4.4 ± 1.4 vs. 4.6 ± 1.5 (p-value = 0.03) for attitude questions. The prevalence of schistosomiasis correlated positively with age, (p-value = 0.049), sex (relative risk = 1.7, p-value < 0.001), and location. Semi-urban locations (n = 382) had higher disease prevalence than urban locations (n = 242), (22.7% vs. 5.5%, p-value < 0.001). Students residing in semi-urban areas and close to a river (<500 m) were at higher risk of contracting schistosomiasis than those living in urban areas far from the river (RR = 5.95, p-value < 0.001). Finally, a correlation between prevalence and proximity of schools to rivers was found (semi-urban areas; RR = −0.91, p-value = 0.001 vs. urban areas; RR = −0.51, p-value = 0.001). Soil-transmitted-helminths prevalence in 2009 was 8.1% and declined during the intervention years to 0.5%. Prevalence in 2018 was found to be stable at 0.8%. These results demonstrate the long-term success of NALAs’ comprehensive model of intervention for elimination of schistosomiasis in school children, combining behavioral change and improved sanitation with MDA. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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12 pages, 2776 KiB

Open AccessArticle

First Molecular Identification of Bulinus africanus in Lake Malawi Implicated in Transmitting Schistosoma Parasites

by Mohammad H. Alharbi, Cynthia Iravoga, Sekeleghe A. Kayuni, Lucas Cunningham, E. James LaCourse, Peter Makaula and J. Russell Stothard

Trop. Med. Infect. Dis. 2022, 7(8), 195; https://doi.org/10.3390/tropicalmed7080195 - 19 Aug 2022

Cited by 7 | Viewed by 2612

Abstract

The freshwater snail genus Bulinus plays a vital role in transmitting parasites of the Schistosoma haematobium group. A hybrid schistosome between S. haematobium and S. mattheei has been recently detected using DNA-based identification methods in school children along the Lake Malawi shoreline in Mangochi District. This finding raised the need for contemporary revaluation of local interactions between schistosomes and snails, with a particular focus on snail species within the Bulinus africanus group. In 2017 and 2018, malacological surveys sampled several freshwater sites in Mangochi District. Collected snails (n = 250) were characterised using cytochrome oxidase subunit 1 gene (cox1), with DNA barcoding of the ‘Folmer’ region and a rapid PCR-RFLP typing assay with double digestion with HaeIII and SacI restriction enzymes. DNA cox1 sequence analysis, with phylogenetic tree construction, suggested the presence of at least three B. africanus group taxa in Lake Malawi, B. globosus, alongside first reports of B. africanus and B. angolensis, which can be differentiated by PCR-RFLP methods. In addition, a total of 30 of the 106 B. africanus group snails (28.30%) were positive to the Schistosoma-specific screen using real-time PCR methods. This study provides new insight into the recent changes in the epidemiology of urogenital schistosomiasis as likely driven by a new diversity of B. africanus group snails within the Lake. Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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7 pages, 274 KiB

Open AccessEditor’s ChoiceOpinion

Human Schistosomiasis Vaccines as Next Generation Control Tools

by Peter J. Hotez and Maria Elena Bottazzi

Trop. Med. Infect. Dis. 2023, 8(3), 170; https://doi.org/10.3390/tropicalmed8030170 - 14 Mar 2023

Cited by 6 | Viewed by 4725

Abstract

Human schistosomiasis remains one of the most important yet neglected tropical diseases, with the latest estimates from the Global Burden of Disease Study indicating that over 140 million people are infected with schistosomes [...] Full article

(This article belongs to the Special Issue Schistosomiasis in Endemic Countries and in Travelers—Two Sides of the Same Coin)

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