Helminth infections were common in medieval Europe and now infect around 1.5 billion people worldwide

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Although helminth infections – including tapeworms and roundworms – are among the world’s top neglected diseases, they are no longer endemic in Europe.

However, researchers reporting in PLOS Neglected Tropical Diseases report that these infections were common in Medieval Europe, according to grave samples analyzed from across the continent.

Helminths are parasitic worms and they infect an estimated 1.5 billion people worldwide.

The worms are transmitted through eggs that are present in human feces and can contaminate soil and water.

While some infections cause only mild symptoms, others are associated with chronic malnutrition and physical impairment, particularly in children.

In the new work, Adrian Smith of the University of Oxford, UK, and colleagues analyzed 589 grave samples from 7 European sites dated between 680 and 1700 CE. Samples were taken from the pelvises of skeletons.

Data associated with the sites allowed them to assess the influence of age, sex and community size on helminth infection rates.

Two soil transmitted nematodes – Ascaris spp. and Trichuris trichiura – were identified at all locations, and two food derived cestodes – Diphyllobothrium latum and Taenia spp. – were found at 4 sites.

No helminths were found in any control samples.

The rates of nematode infection in the medieval population were estimated at 8.5% (range 1.5%-25.6%) for T. trichiura and 25.1% (range 9.3%-42.9%) for Ascaris, similar rates to those seen in modern endemically infected populations.

There were no differences in infection rates by sex or community population size, but infection rates were most common among children.

“Since the prevalence of medieval soil transmitted helminth infections mirror those in modern endemic countries, the factors affecting helminth decline in Europe may also inform modern intervention campaigns,” the researchers say.

“The parasites in past communities can tell us a lot about living conditions including hygiene, sanitation and even culinary practices.”


There are four main nematode species of human soil-transmitted helminth (STH) infections, also known as geohelminths: Ascaris lumbricoides (roundworm), Trichuris trichiura (whipworm), Ancylostoma duodenale and Necator americanus (hookworms).

These infections are most prevalent in tropical and sub-tropical regions of the developing world where adequate water and sanitation are lacking, with recent estimates suggesting that A. lumbricoides infects 1,221 million people, T. trichiura 795 million, and hookworms 740 million (de Silva et al., 2003). The greatest numbers of STH infections occur in sub-Saharan Africa, East Asia, China, India and South America.

Chronic and intense STH infections can contribute to malnutrition and iron-deficiency anaemia, and also can adversely affect physical and mental growth in childhood (Drake et al., 2000; Stephenson et al., 2000; Hotez et al., 2004).

In recognition of the global health importance of STH infections, there is a renewed global commitment to finance and implement control strategies to reduce the disease burden of STH and other helminths, including schistosomiasis (Fenwick et al., 2003), filariasis and onchocerciasis (Molyneux et al., 2003).

The development of effective helminth control is possible because of the availability of proven, cost-effective and logistically feasible intervention strategies. In the case of STH infections, regular periodic chemotherapy, using benzimidazole anthleminthics, of school-aged children delivered through the school system is the main intervention strategy (Aswashi et al., 2004; Hotez et al., 2005; Bundy et al., 2005).

Understanding where at-risk populations live is fundamental for appropriate resource allocation and cost-effective control. In particular, it allows for reliable estimation of the overall drug needs of programmes and efficient geographical targeting of control efforts (Brooker & Michael, 2000).

The precise global distribution of STH infection and how many people are infected and at risk of morbidity however remains poorly defined. This limits how national governments and international organizations define and target resources to combat the disease burden due to STH infection.

A previous review in this series highlighted the potential use of Geographical Information Systems (GIS) and remote sensing (RS) to better understand helminth distributions and their ecological correlates, but also to serve as geographic decision-making tools for identifying areas of particular risk as well as for the design, implementation and monitoring of control programmes (Brooker & Michael, 2000).

As an increasing number of large-scale control efforts are underway, it is timely to assess how the potential of GIS and RS to guide control has been realized in practice. This article begins by describing the scientific basis of how environmental factors affect the biology and transmission dynamics of STH infection.

We then show how satellite data can be used to establish and predict species-specific distributions, and how these tools can help shed additional light on the ecology and epidemiology of infection. Next, we describe how these tools have been effectively used within the context of large-scale control programmes.

Finally, we adopt a data-driven approach to map the contemporary global distributions of STH infection, and relate these to global human population distribution data to derive regional and national estimates of population at risk by parasite species. Although focusing on STH infections, examples will also be presented for other helminthiases, including schistosomiasis, filariasis and onchocerciasis.

Transmission dynamics and the environment

To understand and ultimately predict the global distribution of STH infections it is essential to appreciate their biology, ecology and transmission dynamics. The life cycles of STH infection follow a general pattern.

The adult parasite stages inhabit some part of the host intestine (A. lumbricoides and hookworm in the small intestine; T. trichiura in the colon), reproduce sexually and produce eggs, which are passed in human faeces and deposited in the external environment.

Adult worms survive for several years and produce large numbers of eggs after 4–6 weeks (Table 1).

Eggs can remain viable in the soil for several months (A. lumbricoides and T. trichiura) and larvae several weeks (hookworms), dependent on prevailing environmental conditions. A. duodenale larvae can undergo hypobiosis (arrested development at a specific point in the nematode life cycle) in the human body under certain environmental conditions for several months.

Infection occurs through accidental ingestion of eggs (A. lumbricoides and T. trichiura) or penetration of the skin (by hookworm larvae).

As is common for infectious diseases, the transmission of STH infections can be summarized by the basic reproductive number (R0). This is defined as the average number of female offspring produced by one adult female parasite that attain reproductive maturity, in the absence of density dependent constraints (Anderson & May, 1991).

R0 values of between 1 and 6 are estimated, with rates intrinsically highest for T. trichiura and lowest for hookworm. In practice, epidemiological studies fail to differentiate between the main hookworm species, A. duodenale and N. americanus, which will have different epidemiological and ecological characteristics.

Increases in R0 give rise to increases in infection prevalence (percentage of individuals infected) and infection intensity (number of worms per human host). The dynamic processes involved in STH transmission, such as free-living infective stage development and survival, depend on the prevailing environmental conditions (Pavlovsky, 1966; Anderson, 1982).

For example, as indicated in Figure 1, free-living infective stages present in the environment develop and die at temperature-dependent rates. Maximum survival rates of hookworm larvae, as indicated by proportion of larvae surviving, occur at 20-30 °C (Figure 1a).

Experimental studies suggest that maximum development rates of free-living infective stages occur at temperatures between 28 and 32 °C, with development of A. lumbricoides and T. trichiura arresting below 5 and above 38 °C (Beer, 1976; Seamster, 1950), and development of hookworm larvae ceasing at 40 °C (Udonsi & Atata, 1987; Smith & Schad, 1989) (Figure 1b).

It is suggested that A. lumbricoides eggs are more resistant to extreme temperatures than T. trichiura eggs (Bundy & Cooper, 1989).

Soil moisture and relative atmospheric humidity are also known to influence the development and survival of ova and larvae: higher humidity is associated with faster development of ova; and at low humidity (<50%) the ova of A. lumbricoides and T. trichiura do not embryonate (Otto, 1929; Spindler, 1929).

Field studies show that the abundance of hookworm larvae is related to atmospheric humidity (Nwosu and Anya, 1980; Udonsi et al., 1980).

These differing rates of development and survival will influence parasite establishment in the human host and hence the infection levels. Thus, a climate-induced increase in the rate of establishment, while holding parasite mortality constant, causes the parasite equilibrium to rise (Bundy & Medley, 1992).

Although seasonal dynamics in transmission may occur, such fluctuations may be of little significance to the overall parasite equilibrium within communities. This is because the life-span of adult worms is typically much longer (1-10 years) than the periods in the year during which Ro is less than unity, and Ro will on average will be greater than one, maintaining overall endemicity (Anderson, 1982).

For all these reasons, spatial variability in long-term synoptic environmental factors will have a greater influence on transmission success and patterns of STH infection than seasonal variability in a location.

Urbanization

In common with many other parasitic infections, STH infections flourish in impoverished areas characterized by inadequate sanitation and overcrowding. It is commonly assumed that

A. lumbricoides and T. trichiura are more prevalent in urban areas whereas hookworm is more often found in rural areas (Crompton & Savioli, 1993). However, comparable data STH infections in urban and rural settings are remarkably few and those that do exist indicate a more complicated picture.

Studies which surveyed similar age groups and socio-economic areas indicate that the prevalence of A. lumbricoides and T. trichiura differ between urban and rural communities, but in no systematic manner (Table 2). By contrast, hookworm appears to be equally prevalent in both urban and rural settings (Table 2).

Prevalence of soil-transmitted helminth infections among schoolchildren in urban and rural communities in developing countries. Included studies sought to restrict investigation to areas of similar socio-economic characteristics

The precise reasons for the urban-rural dichotomies for A. lumbricoides and T. trichiura are as yet unclear. Differences in prevalence of A. lumbricoides and T. trichiura in urban and rural areas may reflect differences in sanitation or population density; socio-economic differences will also play an important role. It is clear that further work is needed to resolve these issues.

By 2007, it is predicted that more than half of the global human population will be urban citizens, most of them living in the rapidly growing cities of Africa, Asia and Latin America (United Nations, 2003). Urbanization often accompanies social and economic development, with better opportunities for education, adequate living standards and higher incomes.

However, overcrowding and lack of adequate water and sanitation of urban slum communities may increase transmission of STH infections. Investigation of the impact of increased urbanisation on STH infections together with assessment of the effectiveness of urban helminth control measures in low-income settings is clearly warranted as increased urbanization may promote the transmission of STH infections, especially A. lumbricoides and T. trichiura.


More information: lammer PG, Ryan H, Preston SG, Warren S, P?ichystalová R, et al. (2020) Epidemiological insights from a large-scale investigation of intestinal helminths in Medieval Europe. PLOS Neglected Tropical Diseases 14(8): e0008600. doi.org/10.1371/journal.pntd.0008600

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