• 1.

    Colley DG, Bustinduy AL, Secor WE, King CH, 2014. Human schistosomiasis. Lancet 383: 22532264.

  • 2.

    Fenwick A 2009. The Schistosomiasis Control Initiative (SCI): rational, development and implementation from 2002–2008. Parasitology 136: 17191730.

    • Search Google Scholar
    • Export Citation
  • 3.

    Webster JP, Molyneux DH, Hotez PJ, Fenwick A, 2014. The contribution of mass drug administration to global health – past, present and future. Philos Trans R Soc Lond B Biol Sci 369: 20130434.

    • Search Google Scholar
    • Export Citation
  • 4.

    WHO, 2012. A Roadmap to Elmination. Geneva, Switzerland: World Health Organization.

  • 5.

    WHO, 2013. Schistosomiasis: Progress Report 2001–2011 and Strategic Plan 2012–2020. Geneva, Switzerland: World Health Organization.

  • 6.

    Sokolow SH, Wood CL, Jones IJ, Swartz SJ, Lopez M, Hsieh MH, Lafferty KD, Kuris AM, Rickards C, De Leo GA, 2016. Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Negl Trop Dis 10: e0004794.

    • Search Google Scholar
    • Export Citation
  • 7.

    Shiff C, 2017. Why reinvent the wheal. Lessons in schistosomiasis control from the past. PLoS Negl Trop Dis 11: e0005812.

  • 8.

    Wood CL 2019. Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission. Proc Natl Acad Sci U S A 116: 2318223191.

    • Search Google Scholar
    • Export Citation
  • 9.

    Lamberton PHL, Kabetereine N, Ogutu D, Fenwick A, Webster JP, 2014. Sensitivity and specificity of multiple Kato-Katz thick smears and a circulating cathodic antigen test for Schistosoma mansoni diagnosis pre- and post-repeated praziquantel treatment. PLoS Negl Trop Dis 8: e3139.

    • Search Google Scholar
    • Export Citation
  • 10.

    van Lieshout L, Polderman AM, Deelder AM, 2000. Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Trop 77: 6980.

    • Search Google Scholar
    • Export Citation
  • 11.

    van Dam GJ, Wichers JH, Ferreira TM, Ghati D, van Amerongen A, Deelder AM, 2004. Diagnosis of schistosomiasis by reagent-strip test for detection of circulating cathodic antigen. J Clin Microbiol 42: 54585461.

    • Search Google Scholar
    • Export Citation
  • 12.

    Colley DG 2013. A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosomiasis mansoni. Am J Trop Med Hyg 88: 426432.

    • Search Google Scholar
    • Export Citation
  • 13.

    Tchuenté L-A, Rollinson D, Stothard JR, Molineux D, 2017. Moving from control to elimination of schistosomiasis in sub-Saharan Africa: time to change and adapt strategies. Infect Dis Poverty 6: 42.

    • Search Google Scholar
    • Export Citation
  • 14.

    Bergquist R, Zhou X-N, Rollinson D, Reinhard-Rupp J, Klohe K, 2017. Elimination of schistosomiasis: the tools required. Infect Dis Poverty 6: 158.

  • 15.

    Lo NC 2017. A call to strengthen the global strategy for schisrosomiasis and soil-transmitted helminthiasis: the time is now. Lancet Inf Dis 17: e64e69.

    • Search Google Scholar
    • Export Citation
  • 16.

    Fonseca CT, Oliviera SC, Alves CC, 2015. Elimination of schistosoma by vaccination; what are the best weapons. Front Immunol 6: 95.

  • 17.

    Secor WE, 2014. Water-based interventions for schistosomiasis control. Pathog Glob Health 108: 246254.

  • 18.

    King CH, Bertsch D, 2015. Historical perspective: snail control to prevent schistosomiasis. PLoS Negl Trop Dis 9: e0003657.

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    Knopp S 2012. Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health 12: 930.

    • Search Google Scholar
    • Export Citation
  • 20.

    Chu KY, 1978. Trials of ecological and chemical measures for the control of Schistosoma haematobium transmission in a Volta Lake village. Bull World Health Organ 56: 313322.

    • Search Google Scholar
    • Export Citation
  • 21.

    Kariuki HC, Madsen H, Ouma JH, Butterworth AE, Dunne DW, Booth M, Kimani G, Mwrtha JK, Muchiri E, Venervald BJ, 2013. Long term study on the effect of mollusciciding with niclosamide in stream habitats on transmission of Schistosoma mansoni after community based chemotherapy in Makueni district, Kenya. Parasit Vectors 6: 107.

    • Search Google Scholar
    • Export Citation
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    Jullien M, 2013. Using Pawns to Battle a Killer Disease in Senegal. Africa: BBC News. Available at: http//www.bbc.co/news/world-africa-21080224.

    • Search Google Scholar
    • Export Citation
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    Hofkin BV, Mkoji GM, Koech DK, Loker ES, 1991. Control of schistosome transmitting snails in Kenya by the North American crayfish Procambarus clarkia. Am J Trop Med Hyg 45: 339344.

    • Search Google Scholar
    • Export Citation
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    Mkoji GM 1999. Impact of the crayfish Procambarus clarkii on Schistosoma haematobium transmission in Kenya. Am J Trop Med Hyg 61: 751759.

    • Search Google Scholar
    • Export Citation
  • 25.

    Sleigh A, Li X, Jackson S, Huang K, 1998. Eradication of schistosomiasis in Guangxi, China. Part I: setting, strategies, operations, and outcomes. 1953–92. Bull World Health Organ 76: 361372.

    • Search Google Scholar
    • Export Citation
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    Pointier JP, Jourdane J, 2000. Biological control of the snail hosts of schistosomiasis in areas of low transmission: the example of the Caribbean area. Act Trop 77: 5360.

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    Hamburger J, Abbasi I, Kariuki C, Wanjala A, Mzungu E, Mungai P, Muchiri E, King CH, 2013. Evaluation of loop-mediated isothermal amplification suitable for molecular monitoring of schistosome-infected snails in field laboratories. Am J Trop Med Hyg 88: 344351.

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Molecular Tools and Schistosomiasis Transmission Elimination

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  • 1 Department of Microbiology and Molecular Genetics, The Kuvin Center for the Study of Infectious and Tropical Diseases, The Hebrew University of Jerusalem, Hadassah Medical School, Jerusalem, Israel

Large-scale control efforts in sub-Saharan Africa may leave long-term lingering transmission. Large-scale screening of snail infection prevalence by loop-mediated isothermal amplification will enable accurate determination of man-to-snail transmission, as well as the effects of biota in snail habitat on host capacity and thus on snail-to-man transmission. Next-generation sequencing will enable identification of gut content of snails and thus their feeding preferences in hot spots and in non–hot spots, as well as for identification of attractive vegetation types for attracting snails to molluscicides.

INTRODUCTION

Schistosomiasis, afflicting more than 240 million people,1 is undergoing control across much of south Saharan Africa (SSA).2,3 Complete interruption of transmission of schistosomiasis was also targeted in selected regions by 2025.4,5 Snail control added to public chemotherapy alone6 was applied quite successfully even before the onset of mass administration of praziquantel (PZQ),7 and its importance is increasingly recognized.8

In certain SSA countries, schistosomiasis transmission may linger for a considerable time after repeated mass control activities. Its duration can be expected to depend on human activities and on control input, which may require examination of additional concepts and technologies.

MEDICAL ASPECTS

These came first in control efforts, given existing mass infection and morbidity, which required mass diagnosis, initially by detecting ova in excreta and subsequently by detecting circulating antigens (circulating anodic antigen [CAA] and circulating cathodic antigen [CCA]) in blood and urine.911 This was later used for large-scale screening of the Schistosoma mansoni infection rate by using reagent strips.12 Reduction of infection and morbidity was achieved by repeated mass drug administration (MDA), but it did not stop transmission. This was achieved only in a limited part of the wide distribution area but not in SSA, where infection is the most prevalent.24,6,13 Moreover, reduction of prevalence can return in some areas to high levels when stopping repeated MDA.14,15

SCHISTOSOMIASIS TRANSMISSION ELIMINATION

Vaccination is considered a preferred approach for this purpose, and investigational efforts continue on this line, but an effective and applicable human vaccine is not yet available.16 Alternative means are based on human behavior, clean water supplies, and facilities for removing sewage.

The most sought-after control means were those directed toward reduction of snail populations.17 Niclosamide, available commercially as Bayluscide, is used for large-scale mollusciciding,18 and in certain areas, when combined with the use of PZQ treatment led to an enhanced control effect.6,1921 Introduction of certain species of crayfish feeding on snails2224 was also successful in eliminating snails, but a large-scale application requires further investigation in various types of water bodies. Removal of vegetation on which snails feed was also attempted successfully25,26 but cannot be considered for large-scale control.

Mass screening of snail infection rate is required as long as transmission continues, and the loop-mediated isothermal amplification (LAMP) was suggested for this purpose27 and later actually tested for large-scale screening.28 Loop-mediated isothermal amplification will identify all infected snails, as did PCR, whether shedding cercariae or not.27,28 Identification of snail-to-man transmission, and vice versa, traditionally relied on the identification of snails shedding cercariae. Identification of cercarial shedding is still required for identification of transmission spots from snails to man, especially hot spots (see the following texts). If LAMP is established for large-scale and repeated detection of infected snails, the relation between diagnosis in snails and in humans will require reexamination for determining the desired timing of each. Also, the strategy for diagnosis in humans with different levels of water contact13,29 requires reevaluation toward replacing mass diagnosis and MDA by a more focused choice of target groups.

LOOKING CLOSER AT SNAILS

Factors which affect transmission and its elimination require a closer look at snails and on biota coexisting with them in the habitat. Satellite-based remote sensing contributed to a broad outlook on factors affecting transmission, including water flow, water temperature, and coverage by vegetation.30 Drone-based remote sensing was used to identify vegetation types, and floating and nonemergent vegetation types shown to cause formation of snail clusters were detected. This provided a habitat proxy for high transmission and suggested the effect of vegetation on transmission intensity.8 In the future, development of drone-carried sensors suitable for detecting snails’ life signals may enable a direct mass identification of snail density in transmission sites. This will enable targeting snails by molluscicides, as reported for identifying mosquito larvae, hosts of Plasmodium.31 Until this is realized, other approaches for focal snail control must be sought (as suggested in the following).

When environmental factors affecting transmission by snails take the lead in control activities, snails show characteristics of a pest and should be treated as such. The example of Trichobilharzia spp. present in many water resorts can be more easily perceived as a pest causing cercarial dermatitis in humans.32 But snails transmitting schistosomes are no less pests than mosquitoes transmitting malaria parasites, in terms of intensive human exposure under natural living conditions. Pest control is usually a repeated struggle for controlling the density of pests, preferably with the participation of the affected population (see the following texts).

MASS DETECTION OF INFECTED SNAILS BY LAMP27,28

This is very simple to apply if the complex amplification mixtures used for it (including DNA polymerase, amplification primers, nucleotides, and buffer components) are provided to field laboratories ahead of time and stored until used.27 Determination of prevalence by testing pools of snails will further facilitate these tests.28 Loop-mediated isothermal amplification is particularly important for identifying lingering or resurgent transmission, with a low prevalence of infected snails. Differentiation between snails infected by human schistosomes and those infected by animal schistosomes is also possible by molecular tools.33,34 PCR, the molecular tool preceding LAMP,35,36 was usually rejected for field studies, as it depended on high and expensive technology and on molecular biology know-how.

SNAIL-TO-MAN TRANSMISSION CAPACITY

This appears to be affected by snails’ habitat and can now be identified by using molecular tools. Previously, it was reported that certain species of vegetation and other biota in snails’ habitat can affect transmission to man. It was, thus, shown that water lilies37 and rice38 affect snail abundance and support increased cercarial numbers in the corresponding sites. On the other hand, attachment of rotifers to snails inhibits development of schistosomes within them and reduces the viability of cercariae.39,40 In the case of inhibited development of schistosomes within snails, the availability of molecular monitoring of infected snails at prepatency35 will enable the detection of factors affecting host capacity in the laboratory and in nature. In practice, cercarial shedding is the indicator of the actual snail-to-man transmission. However, without molecular screening, for detecting host capacity of snails, the lack of cercarial shedding can be mistaken for cessation or reduction of man-to-snail transmission.

A year-long screening of infected snails was carried out in which snails were collected at 2-week intervals and examined by both cercarial shedding and by PCR.41 Infected snails were identified by PCR in every snail batch collected from all sites (a total of 19 sites in coastal Kenya) for the whole year, but in several sites, detection by cercarial shedding was not shown at all during this period, or was very rare. This study brings to our attention a condition of “cold spots,” as opposed to the well-known hot spots of transmission (see the following texts). The prevalence of such “cold spots” in endemic areas and their effect on transmission intensity need to be examined at multiple sites, and at shorter time intervals, before and after application of MDA. This is required to evaluate how common this phenomenon is and for seeking out environmental factors that may affect its formation.

Although the matter of “cold spots” needs to be further examined and established, the reality of hot spots is known for years and recognized as a very important factor responsible for persistent transmission after MDA.42 Measurement of cercarial shedding can reveal the presence of hot spots where infected snails shedding cercariae are present in especially large numbers and human infection rates are higher than those in nearby “non–hot spots” after MDA.8,42 When looking at transmission intensity in a wide sense, the terms hot spots, non–hot spots, and “cold spots” are expressions of snail-to-man transmission intensity. “Cold spots” are actually non–hot spots with especially low cercarial shedding, and the clarification of this situation requires further molecular testing of snail capacity in hot spots and in a range of non–hot spots, where different rates of cercarial shedders are found. Various factors relating to nearby human populations were mentioned regarding the formation of hot spots,8,42 and information on the relations between snails and their habitat (types of vegetation) in promoting hot spots was recently addressed.8 Also, the detection of snail clusters by counting snails in the environment8 can suggest attraction of snails to preferred vegetation types, which can be regarded as relevant for developing the concept of the bait principle for focused mollusciciding. Further search of environmental predictors of persistent hot spots was recently presented,43 based on further environmental factors and related factors. Although the vicinity of transmission sites to agricultural plots was mentioned in this study, the identity of the vegetation types in these plots and the possibility that any of them reached the concerned transmission sites and struck roots were not elaborated on. The use of the relatively new molecular tool, the new-generation sequencing (NGS), can be useful for identifying the gut contents of snails, as was performed in sand flies, hosts of Leishmania,44 and thus provide answers to the feeding preferences of snails from each of the spots mentioned earlier.

A FOCUSED APPLICATION OF MOLLUSCICIDES

This is required for increasing mollusciciding efficiency by directing it to sites with high snail abundance. Feeding preference of snails, as determined by NGS, opens up the gate for examining the bait principle for attracting snails to a mollusciciding environment. Testing of this principle in the laboratory clearly demonstrated that the combination between L-glutamine and a slow release polymeric formulation (calcium alginate beads) of niclosamide had a strong attraction and mollusciciding effect.45 In addition to L-glutamine, several other amino acids were also identified as attractive for snails (cited in Refs. 45 and 46), and certain other compounds such as starch and glycogen were also found to be attractive for snails.47 These experiments indicated that the combination between an attractant (bait) and niclosamide does not deter snails from being attracted and then killed. In other experiments, it was further shown that Biomphalaria glabrata snails are attracted or trapped by minced lettuce,48 thus demonstrating the potential of vegetation items as snail baits. The combination of attractive vegetation and molluscicides can be expected to be less costly and easier to produce for application on a large scale. Such a formula is potentially suitable as “pest control” used with the participation of exposed populations.

Agricultural plants with leaves have leftovers which may be available for examining their attraction for snails. The information on vegetation preference by snails awaits laboratory studies comparing snails growing on Romanian lettuce, the common feeding vegetation in the laboratory, with a variety of agricultural products that may be considered as potential baits. If indeed attractive, these vegetation types when distributed in suitable spots are expected to cause clustering of snails around them. The use of NGS44,49 can provide identification of snails’ feeding preferences. The potential usefulness of a bait–niclosamide combination requires that molluscicides can be attached to attractive vegetation species, as is being widely applied in agriculture for attaching fertilizers.50 Bait-based control can be considered to be sound as a combination of attractive L-arginine and niclosamide does not deter snails from being attracted to the molluscicide.45 Various possible industrial products of vegetation–molluscicide combination can be considered, according to optimal distribution and efficacy strategies.

REFERENCES

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    Colley DG, Bustinduy AL, Secor WE, King CH, 2014. Human schistosomiasis. Lancet 383: 22532264.

  • 2.

    Fenwick A 2009. The Schistosomiasis Control Initiative (SCI): rational, development and implementation from 2002–2008. Parasitology 136: 17191730.

    • Search Google Scholar
    • Export Citation
  • 3.

    Webster JP, Molyneux DH, Hotez PJ, Fenwick A, 2014. The contribution of mass drug administration to global health – past, present and future. Philos Trans R Soc Lond B Biol Sci 369: 20130434.

    • Search Google Scholar
    • Export Citation
  • 4.

    WHO, 2012. A Roadmap to Elmination. Geneva, Switzerland: World Health Organization.

  • 5.

    WHO, 2013. Schistosomiasis: Progress Report 2001–2011 and Strategic Plan 2012–2020. Geneva, Switzerland: World Health Organization.

  • 6.

    Sokolow SH, Wood CL, Jones IJ, Swartz SJ, Lopez M, Hsieh MH, Lafferty KD, Kuris AM, Rickards C, De Leo GA, 2016. Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Negl Trop Dis 10: e0004794.

    • Search Google Scholar
    • Export Citation
  • 7.

    Shiff C, 2017. Why reinvent the wheal. Lessons in schistosomiasis control from the past. PLoS Negl Trop Dis 11: e0005812.

  • 8.

    Wood CL 2019. Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission. Proc Natl Acad Sci U S A 116: 2318223191.

    • Search Google Scholar
    • Export Citation
  • 9.

    Lamberton PHL, Kabetereine N, Ogutu D, Fenwick A, Webster JP, 2014. Sensitivity and specificity of multiple Kato-Katz thick smears and a circulating cathodic antigen test for Schistosoma mansoni diagnosis pre- and post-repeated praziquantel treatment. PLoS Negl Trop Dis 8: e3139.

    • Search Google Scholar
    • Export Citation
  • 10.

    van Lieshout L, Polderman AM, Deelder AM, 2000. Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Trop 77: 6980.

    • Search Google Scholar
    • Export Citation
  • 11.

    van Dam GJ, Wichers JH, Ferreira TM, Ghati D, van Amerongen A, Deelder AM, 2004. Diagnosis of schistosomiasis by reagent-strip test for detection of circulating cathodic antigen. J Clin Microbiol 42: 54585461.

    • Search Google Scholar
    • Export Citation
  • 12.

    Colley DG 2013. A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosomiasis mansoni. Am J Trop Med Hyg 88: 426432.

    • Search Google Scholar
    • Export Citation
  • 13.

    Tchuenté L-A, Rollinson D, Stothard JR, Molineux D, 2017. Moving from control to elimination of schistosomiasis in sub-Saharan Africa: time to change and adapt strategies. Infect Dis Poverty 6: 42.

    • Search Google Scholar
    • Export Citation
  • 14.

    Bergquist R, Zhou X-N, Rollinson D, Reinhard-Rupp J, Klohe K, 2017. Elimination of schistosomiasis: the tools required. Infect Dis Poverty 6: 158.

  • 15.

    Lo NC 2017. A call to strengthen the global strategy for schisrosomiasis and soil-transmitted helminthiasis: the time is now. Lancet Inf Dis 17: e64e69.

    • Search Google Scholar
    • Export Citation
  • 16.

    Fonseca CT, Oliviera SC, Alves CC, 2015. Elimination of schistosoma by vaccination; what are the best weapons. Front Immunol 6: 95.

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    Secor WE, 2014. Water-based interventions for schistosomiasis control. Pathog Glob Health 108: 246254.

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    King CH, Bertsch D, 2015. Historical perspective: snail control to prevent schistosomiasis. PLoS Negl Trop Dis 9: e0003657.

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    Knopp S 2012. Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health 12: 930.

    • Search Google Scholar
    • Export Citation
  • 20.

    Chu KY, 1978. Trials of ecological and chemical measures for the control of Schistosoma haematobium transmission in a Volta Lake village. Bull World Health Organ 56: 313322.

    • Search Google Scholar
    • Export Citation
  • 21.

    Kariuki HC, Madsen H, Ouma JH, Butterworth AE, Dunne DW, Booth M, Kimani G, Mwrtha JK, Muchiri E, Venervald BJ, 2013. Long term study on the effect of mollusciciding with niclosamide in stream habitats on transmission of Schistosoma mansoni after community based chemotherapy in Makueni district, Kenya. Parasit Vectors 6: 107.

    • Search Google Scholar
    • Export Citation
  • 22.

    Jullien M, 2013. Using Pawns to Battle a Killer Disease in Senegal. Africa: BBC News. Available at: http//www.bbc.co/news/world-africa-21080224.

    • Search Google Scholar
    • Export Citation
  • 23.

    Hofkin BV, Mkoji GM, Koech DK, Loker ES, 1991. Control of schistosome transmitting snails in Kenya by the North American crayfish Procambarus clarkia. Am J Trop Med Hyg 45: 339344.

    • Search Google Scholar
    • Export Citation
  • 24.

    Mkoji GM 1999. Impact of the crayfish Procambarus clarkii on Schistosoma haematobium transmission in Kenya. Am J Trop Med Hyg 61: 751759.

    • Search Google Scholar
    • Export Citation
  • 25.

    Sleigh A, Li X, Jackson S, Huang K, 1998. Eradication of schistosomiasis in Guangxi, China. Part I: setting, strategies, operations, and outcomes. 1953–92. Bull World Health Organ 76: 361372.

    • Search Google Scholar
    • Export Citation
  • 26.

    Pointier JP, Jourdane J, 2000. Biological control of the snail hosts of schistosomiasis in areas of low transmission: the example of the Caribbean area. Act Trop 77: 5360.

    • Search Google Scholar
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Author Notes

Address correspondence to Joseph Hamburger, The Hebrew University of Jerusalem, Hadassah Medical School, P.O.B. 12272, Jerusalem 91120, Israel. E-mail: joseph.hamburger@mail.huji.ac.il

Author’s address: Joseph Hamburger, Department of Microbiology and Molecular Genetics, The Kuvin Center for the Study of Infectious and Tropical Diseases, The Hebrew University of Jerusalem, Hadassah Medical School, Jerusalem, Israel, E-mail: joseph.hamburger@mail.huji.ac.il.

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