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Schistosomiasis: Host-Pathogen Biology

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A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Parasitic Pathogens".

Deadline for manuscript submissions: closed (15 December 2021) | Viewed by 31955

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Prof. Dr. Hannah Wei Wu

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Guest Editor

Center for International Health Research, Rhode Island Hospital, School of Medicine, Brown University, Providence, RI, USA
Interests: schistosomiasis epidemiology; immunology and vaccine development

Special Issue Information

Dear Colleagues,

Schistosomiasis currently infects over 200 million individuals and results in an estimated 2-15% chronic disability which contributes to poor health and economic stagnation in endemic areas. It continues to be one of the leading disease burdens in the endemic regions despite decades of mass chemotherapy with praziquantel. Three principal species of dioecious trematodes (flatworms) infect humans including Schistosoma mansoni, S. haematobium, and S. japonicum.

The mechanisms driving the pathogenesis of schistosomiasis remain elusive. Our knowledge gap in host-pathogen biology has limited the development of efficient diagnosis and effective treatments. Praziquantel treatment is highly efficacious in eliminating the adult worms but not sufficient to revert the lesions. The traditional diagnosis is not sensitive enough for monitoring in regions moving toward disease eradication. To combat the zoonotic schistosomiasis japonica, an animal vaccine may be prioritized under the one health disease control strategy.

Understanding the host-parasite biology, especially the interactions could help us to develop appropriate interventions to control schistosomiasis. In this special issue, we aim to collect a variety of up-to-date articles covering important aspects of schistosomiasis pathogenesis as well as insights in diagnosis and vaccine development. Submission of basic and translational original research and reviews on the following sub-topics are all welcome:

Host-parasite interactions in both lab and field settings.
Host immune responses against Schistosoma spp. and the application of it to disease prevention and control of mortality
Host immune responses and its influence on co-infection and non-communicable diseases including metabolic disorders
Outlook on One Health approach in schistosomiasis prevention and control.
Point-of-care diagnosis tools for active infection.
Biomarkers for disease morbidity and mortality.
Animal models to study schistosomiasis including liver fibrosis, myeloradiculopathy, neural schistosomiasis, urinary and female genital schistosomiasis.
Identifying novel vaccine candidates.
Vaccine trial reports in large animals.

Prof. Dr. Hannah Wei Wu
Guest Editor

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Keywords

schistosomiasis
host-pathogen interaction
immunology
biomarkers
diagnosis
vaccine
One Health

Published Papers (11 papers)

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Research

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15 pages, 7421 KiB

Open AccessEditor’s ChoiceArticle

Population Genetic Structure and Hybridization of Schistosoma haematobium in Nigeria

by Amos Mathias Onyekwere, Olivier Rey, Jean-François Allienne, Monday Chukwu Nwanchor, Moses Alo, Clementina Uwa and Jerome Boissier

Pathogens 2022, 11(4), 425; https://doi.org/10.3390/pathogens11040425 - 31 Mar 2022

Cited by 10 | Viewed by 2375

Abstract

Background: Schistosomiasis is a major poverty-related disease caused by dioecious parasitic flatworms of the genus Schistosoma with a health impact on both humans and animals. Hybrids of human urogenital schistosome and bovine intestinal schistosome have been reported in humans in several of Nigeria’s neighboring West African countries. No empirical studies have been carried out on the genomic diversity of Schistosoma haematobium in Nigeria. Here, we present novel data on the presence and prevalence of hybrids and the population genetic structure of S. haematobium. Methods: 165 Schistosoma-positive urine samples were obtained from 12 sampling sites in Nigeria. Schistosoma haematobium eggs from each sample were hatched and each individual miracidium was picked and preserved in Whatman^® FTA cards for genomic analysis. Approximately 1364 parasites were molecularly characterized by rapid diagnostic multiplex polymerase chain reaction (RD-PCR) for mitochondrial DNA gene (Cox1 mtDNA) and a subset of 1136 miracidia were genotyped using a panel of 18 microsatellite markers. Results: No significant difference was observed in the population genetic diversity (p > 0.05), though a significant difference was observed in the allelic richness of the sites except sites 7, 8, and 9 (p < 0.05). Moreover, we observed two clusters of populations: west (populations 1–4) and east (populations 7–12). Of the 1364 miracidia genotyped, 1212 (89%) showed an S. bovis Cox1 profile and 152 (11%) showed an S. haematobium cox1 profile. All parasites showed an S. bovis Cox1 profile except for some at sites 3 and 4. Schistosoma miracidia full genotyping showed 59.3% of the S. bovis ITS2 allele. Conclusions: This study provides novel insight into hybridization and population genetic structure of S. haematobium in Nigeria. Our findings suggest that S. haematobium x S. bovis hybrids are common in Nigeria. More genomic studies on both human- and animal-infecting parasites are needed to ascertain the role of animals in schistosome transmission. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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11 pages, 1441 KiB

Open AccessArticle

Laboratory Evaluation of a Basic Recombinase Polymerase Amplification (RPA) Assay for Early Detection of Schistosoma japonicum

by Wangping Deng, Shenglin Wang, Liping Wang, Chao Lv, Yinlong Li, Ting Feng, Zhiqiang Qin and Jing Xu

Pathogens 2022, 11(3), 319; https://doi.org/10.3390/pathogens11030319 - 4 Mar 2022

Cited by 6 | Viewed by 3602

Abstract

Early detection of Schistosoma japonicum (S. japonicum) within its intermediate and definitive hosts is crucial for case finding and disease surveillance, especially in low-endemic areas. Recombinase polymerase amplification (RPA) has many advantages over traditional methods of DNA-amplification, such as polymerase chain reaction (PCR), including high sensitivity and specificity whilst being deployable in resource-poor schistosomiasis-endemic areas. Here, we evaluated the performance of a basic RPA assay targeting the 28srDNA gene fragment of S. japonicum (Sj28srDNA) using schistosome-infected Oncomelania hupensis (O. hupensis) and mouse models, compared to the traditional pathological method and a PCR assay. Overall S. japonicum infection prevalence within O. hupensis hosts by microscopic dissection, PCR and RPA was 9.29% (13/140), 32.14% (45/140) and 51.43% (72/140), respectively, presenting significant differences statistically (χ² = 58.31, p < 0.001). It was noteworthy that infection prevalence by PCR and RPA performed was 34.44% (31/90) and 53.33% (48/90) in snails within 6 weeks post-infection, while the dissection method detected all samples as negatives. In addition, the basic RPA assay presented positive results from the fourth week post-infection and third day post-infection when detecting fecal DNA and serum DNA, respectively, which were extracted from a pooled sample from mice infected with 20 S. japonicum cercariae. This study suggests that the RPA assay has high potential for early detection of S. japonicum infection within its intermediate and definitive hosts. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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12 pages, 1383 KiB

Open AccessArticle

Schistosomes Impede ATP-Induced T Cell Apoptosis In Vitro: The Role of Ectoenzyme SmNPP5

by Catherine S. Nation, Akram A. Da'dara, Manal Elzoheiry and Patrick J. Skelly

Pathogens 2022, 11(2), 155; https://doi.org/10.3390/pathogens11020155 - 26 Jan 2022

Cited by 2 | Viewed by 2163

Abstract

Schistosomes (blood flukes) can survive in the bloodstream of their hosts for many years. We hypothesize that proteins on their host-interactive surface impinge on host biochemistry to help ensure their long-term survival. Here, we focus on a surface ectoenzyme of Schistosoma mansoni, designated SmNPP5. This ~53 kDa glycoprotein is a nucleotide pyrophosphatase/phosphodiesterase that has been previously shown to: (1) cleave adenosine diphosphate (ADP) and block platelet aggregation; and (2) cleave nicotinamide adenine dinucleotide (NAD) and block NAD-induced T cell apoptosis in vitro. T cell apoptosis can additionally be driven by extracellular adenosine triphosphate (ATP). In this work, we show that adult S. mansoni parasites can inhibit this process. Further, we demonstrate that recombinant SmNPP5 alone can both cleave ATP and impede ATP-induced T cell killing. As immunomodulatory regulatory T cells (Tregs) are especially prone to the induction of these apoptotic pathways, we hypothesize that the schistosome cleavage of both NAD and ATP promotes Treg survival and this helps to create a less immunologically hostile environment for the worms in vivo. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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18 pages, 824 KiB

Open AccessArticle

Schistosoma mansoni Adult Worm Protective and Diagnostic Proteins in n-Butanol Extracts Revealed by Proteomic Analysis

by Guidenn Sulbarán, Giovani C. Verissimo da Costa, Sandra Losada, José M. Peralta and Italo M. Cesari

Pathogens 2022, 11(1), 22; https://doi.org/10.3390/pathogens11010022 - 24 Dec 2021

Viewed by 2680

Abstract

The S. mansoni adult worm n-butanol extract (Sm-AWBE) has been previously shown to contain specific S. mansoni antigens that have been used for immunodiagnosis of schistosomiasis in solid phase alkaline phosphatase immunoassay (APIA) and western blot (WB) analyses. Sm-AWBE was also used in immunoprotection studies against a fatal live-cercariae challenge in experimental mouse vaccination (~43% protection). The Sm-AWBE fraction was prepared by mixing adult worm membranous suspensions with aqueous-saturated n-butanol, centrifuging and recovering n-butanol-resistant proteins in the aqueous phase. Here we report a preliminary identification of Sm-AWBE protein components as revealed from a qualitative proteomic study after processing Sm-AWBE by 1D-gel electrophoresis, in-gel and in-solution tryptic digestions, and mass spectrometry analyses. We identified 33 proteins in Sm-AWBE, all previously known S. mansoni proteins and antigens; among them, immunomodulatory proteins and proteins mostly involved in host–parasite interactions. About 81.8% of the identified Sm-AWBE proteins are antigenic. STRING analysis showed a set of Sm-AWBE proteins configuring a small network of interactive proteins and a group of proteins without interactions. Functional groups of proteins included muscle contraction, antioxidant, GPI-anchored phosphoesterases, regulatory 14-3-3, various enzymes and stress proteins. The results widen the possibilities to design novel antigen combinations for better diagnostic and immunoprotective strategies for schistosomiasis control. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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11 pages, 707 KiB

Open AccessArticle

Distinct Schistosoma mansoni-Specific Immunoglobulin Subclasses Are Induced by Different Schistosoma mansoni Stages—A Tool to Decipher Schistosoma mansoni Infection Stages

by Kathrin Arndts, Tayseer E. M. Elfaki, Michael J. Doenhoff, Gnatoulma Katawa, Ibtisam A. Goreish, Misk El Yemen A. Atti El Mekki, Achim Hoerauf, Manuel Ritter and Laura E. Layland

Pathogens 2022, 11(1), 19; https://doi.org/10.3390/pathogens11010019 - 24 Dec 2021

Cited by 1 | Viewed by 2610

Abstract

Despite the existence of an effective medication against schistosomiasis, the disease remains a major health problem in affected areas, especially for those lacking appropriate sanitary facilities. Moreover, treatment cannot prevent re-infection since it is only effective on adult schistosome worms. Previous retrospective studies in the Sudan have discovered unique immuno-epidemiological profiles in uninfected individuals and those positive for Schistosoma mansoni via polymerase chain reaction (PCR) but egg-negative and those with eggs in their stool. Expanding on these data, serum samples from these individuals were further investigated for the presence of cercarial (SmCTF)-specific antibodies, which would indicate immune responses at the early stages of infection. Indeed, SmCTF IgG1, 2, 3 and 4 levels were significantly elevated in SmPCR⁺ individuals when compared to egg⁺ patients. Following multivariable regression analysis, including SmCTF-specific Igs, Schistosoma egg antigen (SEA)-specific and Schistosoma worm antigen (SWA)-specific immunoglobulins revealed a specific immunoglobulin (Ig) profile of individuals presenting different states of infection, which may be a useful future tool in order to identify egg⁻ individuals and thereby prevent unnecessary treatments. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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11 pages, 1463 KiB

Open AccessArticle

The Dynamics of Hepatic Fibrosis Related to Schistosomiasis and Its Risk Factors in a Cohort of China

by Fei Hu, Shu-Ying Xie, Min Yuan, Yi-Feng Li, Zhao-Jun Li, Zhu-Lu Gao, Wei-Ming Lan, Yue-Ming Liu, Jing Xu and Dan-Dan Lin

Pathogens 2021, 10(12), 1532; https://doi.org/10.3390/pathogens10121532 - 23 Nov 2021

Cited by 6 | Viewed by 1812

Abstract

China has had a long history against schistosomiasis japonica. The most serious prognosis of chronic schistosome infection is hepatic fibrosis, which develops into advanced schistosomiasis if the process is not effectively controlled. After a more than seven decades endeavor, China has gained remarkable achievements in schistosomiasis control and achieved transmission control nationwide (infection rate of schistosomes in residents and domestic animals both less than 1%) by 2015. However, new advanced schistosomiasis cases emerge annually in China, even in areas where the transmission of schistosomiasis had been interrupted. In the present study, the residents (>5 years old) in a schistosomiasis endemic village were examined for schistosomiasis every year during 1995–2019 by the modified Kato–Katz thick smear method and/or miracidium hatching technique. Residents who were identified to have an active infection method were treated with praziquantel at a dose of 40 mg/kg body weight. Ultrasonography was carried out to assess the liver morbidity related to schistosomiasis in 1995 and 2019, respectively. The prevalence of schistosomiasis among residents presented a downward trend annually, from 17.89% (175/978) in 1995 to 0 (0/475) in 2019. Among 292 residents who received ultrasound scan both in 1995 and 2019, 141 (48.29%) presented stable liver damage, while liver fibrosis was developed severely in 86 (29.45%) and reversed in 65 (22.26%) residents. Univariate and multivariate analysis showed that anti-fibrosis treatment was the protective factor against schistosomiasis hepatic fibrosis. Males, residents aged 38 and above, fishermen, and people who did not receive anti-fibrosis treatment were groups with higher risk of liver fibrosis development. Our results revealed that although the infection rate of schistosome dropped significantly in endemic areas, liver fibrosis was still developing among some residents, even though they had received deworming treatment. Liver protection/anti-fibrosis treatment should be administered in endemic regions and regions with historically uncontrolled transmission to slow down the deterioration of hepatic fibrosis among patients in schistosomiasis endemic areas. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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11 pages, 7599 KiB

Open AccessArticle

Bulinus senegalensis and Bulinus umbilicatus Snail Infestations by the Schistosoma haematobium Group in Niakhar, Senegal

by Papa Mouhamadou Gaye, Souleymane Doucoure, Bruno Senghor, Babacar Faye, Ndiaw Goumballa, Mbacké Sembène, Coralie L’Ollivier, Philippe Parola, Stéphane Ranque, Doudou Sow and Cheikh Sokhna

Pathogens 2021, 10(7), 860; https://doi.org/10.3390/pathogens10070860 - 8 Jul 2021

Cited by 5 | Viewed by 2938

Abstract

Thorough knowledge of the dynamics of Bulinus spp. infestation could help to control the spread of schistosomiasis. This study describes the spatio-temporal dynamics of B. senegalensis and B. umbilicatus infestation by the Schistosoma haematobium group of blood flukes in Niakhar, Senegal. Molecular identification of the S. haematobium group was performed by real-time PCR, targeting the Dra 1 gene in 810 samples of Bulinus spp. collected during the schistosomiasis transmission season in 2013. In addition to Dra 1 PCR, a rapid diagnostic-PCR was performed on a sub-group of 43 snails to discriminate S. haematobium, S. bovis, and S. mattheei. Out of 810 snails, 236 (29.1%) were positive for Dra 1 based on the PCR, including 96.2% and 3.8% of B. senegalensis and B. umbilicatus, respectively. Among the sub-group, 16 samples were confirmed to be S. haematobium while one was identified as a mixture of S. haematobium and S. bovis. Snails infestations were detected in all villages sampled and infestation rates ranged from 15.38% to 42.11%. The prevalence of infestation was higher in the north (33.47%) compared to the south (25.74%). Snail populations infestations appear early in the rainy season, with a peak in the middle of the season, and then a decline towards the end of the rainy season. Molecular techniques showed, for the first time, the presence of S. bovis in the Bulinus spp. population of Niakhar. The heterogeneity of snail infestations at the village level must be taken into account in mass treatment strategies. Further studies should help to improve the characterizations of the schistosome population. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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Review

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18 pages, 692 KiB

Open AccessReview

Molecular Techniques as Alternatives of Diagnostic Tools in China as Schistosomiasis Moving towards Elimination

by Chao Lv, Wangping Deng, Liping Wang, Zhiqiang Qin, Xiaonong Zhou and Jing Xu

Pathogens 2022, 11(3), 287; https://doi.org/10.3390/pathogens11030287 - 24 Feb 2022

Cited by 14 | Viewed by 3784

Abstract

Schistosomiasis japonica caused by the trematode flukes of Schistosoma japonicum was one of the most grievous infectious diseases in China in the mid-20th century, while its elimination has been placed on the agenda of the national strategic plan of healthy China 2030 after 70 years of continuous control campaigns. Diagnostic tools play a pivotal role in warfare against schistosomiasis but must adapt to the endemic status and objectives of activities. With the decrease of prevalence and infection intensity of schistosomiasis in human beings and livestock, optimal methodologies with high sensitivity and absolute specificity are needed for the detection of asymptomatic cases or light infections, as well as disease surveillance to verify elimination. In comparison with the parasitological methods with relatively low sensitivity and serological techniques lacking specificity, which both had been widely used in previous control stages, the molecular detection methods based on the amplification of promising genes of the schistosome genome may pick up the baton to assist the eventual aim of elimination. In this article, we reviewed the developed molecular methods for detecting S. japonicum infection and their application in schistosomiasis japonica diagnosis. Concurrently, we also analyzed the chances and challenges of molecular tools to the field application process in China. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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14 pages, 870 KiB

Open AccessReview

Development of New Technologies for Risk Identification of Schistosomiasis Transmission in China

by Liang Shi, Jian-Feng Zhang, Wei Li and Kun Yang

Pathogens 2022, 11(2), 224; https://doi.org/10.3390/pathogens11020224 - 8 Feb 2022

Cited by 2 | Viewed by 1765

Abstract

Schistosomiasis is serious parasitic disease with an estimated global prevalence of active infections of more than 190 million. Accurate methods for the assessment of schistosomiasis risk are crucial for schistosomiasis prevention and control in China. Traditional approaches to the identification of epidemiological risk factors include pathogen biology, immunology, imaging, and molecular biology techniques. Identification of schistosomiasis risk has been revolutionized by the advent of computer network communication technologies, including 3S, mathematical modeling, big data, and artificial intelligence (AI). In this review, we analyze the development of traditional and new technologies for risk identification of schistosomiasis transmission in China. New technologies allow for the integration of environmental and socio-economic factors for accurate prediction of the risk population and regions. The combination of traditional and new techniques provides a foundation for the development of more effective approaches to accelerate the process of schistosomiasis elimination. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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12 pages, 266 KiB

Open AccessReview

From the One Health Perspective: Schistosomiasis Japonica and Flooding

by Su-Ying Guo, Lu Li, Li-Juan Zhang, Yin-Long Li, Shi-Zhu Li and Jing Xu

Pathogens 2021, 10(12), 1538; https://doi.org/10.3390/pathogens10121538 - 25 Nov 2021

Cited by 14 | Viewed by 3036

Abstract

Schistosomiasis is a water-borne parasitic disease distributed worldwide, while schistosomiasis japonica localizes in the People’s Republic of China, the Philippines, and a few regions of Indonesia. Although significant achievements have been obtained in these endemic countries, great challenges still exist to reach the elimination of schistosomiasis japonica, as the occurrence of flooding can lead to several adverse consequences on the prevalence of schistosomiasis. This review summarizes the influence of flooding on the transmission of schistosomiasis japonica and interventions responding to the adverse impacts from the One Health perspective in human beings, animals, and the environment. For human and animals, behavioral changes and the damage of water conservancy and sanitary facilities will increase the intensity of water contact. For the environment, the density of Oncomelania snails significantly increases from the third year after flooding, and the snail habitats can be enlarged due to active and passive diffusion. With more water contact of human and other reservoir hosts, and larger snail habitats with higher density of living snails, the transmission risk of schistosomiasis increases under the influence of flooding. With the agenda set for global schistosomiasis elimination, interventions from the One Health perspective are put forward to respond to the impacts of increased flooding. For human beings, conducting health education to increase the consciousness of self-protection, preventive chemotherapy for high-risk populations, supply of safe water, early case finding, timely reporting, and treating cases will protect people from infection and prevent the outbreak of schistosomiasis. For animals, culling susceptible domestic animals, herding livestock in snail-free areas, treating livestock with infection or at high risk of infection, harmless treatment of animal feces to avoid water contamination, and monitoring the infection status of wild animals in flooding areas are important to cut off the transmission chain from the resources. For the environment, early warning of flooding, setting up warning signs and killing cercaria in risk areas during and post flooding, reconstructing damaged water conservancy facilities, developing hygiene and sanitary facilities, conducting snail surveys, using molluscicide, and predicting areas with high risk of schistosomiasis transmission after flooding all contribute to reducing the transmission risk of schistosomiasis. These strategies need the cooperation of the ministry of health, meteorological administration, water resources, agriculture, and forestry to achieve the goal of minimizing the impact of flooding on the transmission of schistosomiasis. In conclusion, flooding is one of the important factors affecting the transmission of schistosomiasis japonica. Multi-sectoral cooperation is needed to effectively prevent and control the adverse impacts of flooding on human beings, animals, and the environment. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

14 pages, 820 KiB

Open AccessReview

Medical Imaging in the Diagnosis of Schistosomiasis: A Review

by Andrea Cimini, Maria Ricci, Paola Elda Gigliotti, Luca Pugliese, Agostino Chiaravalloti, Roberta Danieli and Orazio Schillaci

Pathogens 2021, 10(8), 1058; https://doi.org/10.3390/pathogens10081058 - 20 Aug 2021

Cited by 7 | Viewed by 3681

Abstract

Schistosomiasis is one of the most important parasitic diseases and it is endemic in tropical and subtropical areas. Clinical and laboratory data are fundamental for the diagnosis of schistosomiasis, but diagnostic imaging techniques such as x-rays, ultrasound (US), computed tomography (CT), magnetic resonance imaging (MRI), and positron emission tomography/computed tomography (PET/CT) may be helpful in the evaluation of disease severity and complications. In this context, the aim of this review is to explore the actual role of diagnostic imaging in the diagnosis of schistosomiasis, underlining advantages and drawbacks providing information about the utilization of diagnostic imaging techniques in this context. Furthermore, we aim to provide a useful guide regarding imaging features of schistosomiasis for radiology and nuclear medicine physicians of non-endemic countries: in fact, in the last years non-endemic countries have experienced important flows of migrants from endemic areas, therefore it is not uncommon to face cases of this disease in daily practice. Full article

(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)

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