Pathogenic helminths in the past: Much ado about nothing

Despite a long tradition on the extent to which Romanisation has improved human health, some recent studies suggest that Romanisation in general, and Roman sanitation in particular, may not have made people any healthier, given that in Roman times gastrointestinal parasites were apparently widespread, whilst in the present day such parasites rarely cause diseases. Unfortunately, this novel claim neglects the empirical evidence that worldwide infections in over 1.5 billion people are caused by ubiquitous foodborne nematodes. Therefore, many may wonder if fossil remains of soil-transmitted helminths have been reported in ancient sanitation infrastructures. Beneficial access to improved sanitation should always be prioritized, hence how can historical sanitation efforts have ever been harmful? In this short article, a strong plea for caution is given, asking for an augmented nematological record and showing that there is not any evidence against Roman sanitation, neither in the past nor in the present.

In her Nature feature, Chelsea Wald 1 reviewed some of the conclusions by Piers D. Mitchell 2 and describes the fascinating rise of latrines in Mesopotamia, Greece and the Roman Empire. Both authors tried to point out that most of these sanitation facilities were not doing much for the residents' health, despite the idea that sophisticated plumbing systems, like those of ancient Rome, may have acted as a kind of control that could benefit even the poor. This debated interpretation was based on the fact that human hosts mainly acquire infective nematodes via the faecal-oral route through the soil, although unembryonated eggs can remain viable in the soil for 15 years. Helminth preservation seems to be the highest in moist anaerobic environments like latrines 3 ; therefore, even Roman latrines, with continuous flushing and related sediments (coprolites), can become valuable for the reconstruction of past gastrointestinal infections, if evaluated correctly.
As a matter of fact, water purification will always be one of the most intriguing examples of how public health and societal health are interwoven. Amazing examples come from Roman history, where water and wastewater systems rapidly became pillars for European civilisation. The large-scale introduction by Romans of fountains into or near public buildings, together with closed aqueducts, can be seen as the very first Water Safety Plan. Interestingly, archaeologists somehow seem to be ideologically motivated to conceptualize diseases and outbreaks in Roman times, despite the thin palynological record from ancient sanitation infrastructures around the Mediterranean Sea 1,2 ( Figure 1).
Many pathogens are reported in ancient latrines because they are intrinsically correlated to human settlements, and not to sanitation infrastructures themselves, which are supposed to reduce the risk of contact with outbreak sources. On one hand, it is true that fossil remains of roundworms, whipworms and hookworms (collectively referred to as soil-transmitted helminths) have been reported from ancient sanitation infrastructures. On the other hand, Romans were fully aware of the importance of clean water and efficient sanitation systems. Already during the short reign of

Amendments from Version 2
There are apparently different views on Roman water technology, hence I improved my take-home message on public health. The suggested attempt to explain the historical occurrence of helminth eggs in urban areas by a possible increase of manure application in the countryside is challenging although out of the scope of this communication, but for those interested in that aspect I strongly recommend literature reviews like Dark & Gent in Oxford Journal of Archaeology 20 (2001) Nematodes are the most frequently occurring invertebrates. These primitive soil organisms occupy diverse trophic levels in ecological networks and can act either as antagonists for soilborne pests or be pathogens themselves. It can be dangerous to suggest that sanitation may not have made people any healthier, as humans can also get infected with soil nematodes by ingesting unclean vegetables or by contact with infected domestic animals. Along the aforementioned faecal-oral route, behavioral and allometric factors have been put forward in existing literature 9 , being the host-related factors linked to human size prominent. According to host-parasite regression models for mammals 9 and assuming on average one adult body weight of 62.0 kg (corresponding to a volume of 61,400 cc), each infected human might contain up to 12,300 helminths.
Hence, it is not surprising to find helminths in sanitation systems of ancient settlements, especially if only the palaeoparasitological data for sites at which these pathogens were detected are gathered together. For instance, archaeological records of commonsource outbreaks can be collated to support the idea that sanitation facilities historically linked to Romanisation have widespread helminths, although these cosmopolitan endoparasites are well-known to occur during Roman times even around the Pacific Ocean, including the New World in pre-colonial times 5,7,8,10 ( Figure 1). Thus, we have to realize that there would be many more helminth eggs in ancient sanitation facilities if these facilities had not been there in the past. Surprisingly, archaeologists like to invert this basic framework, and suggestive interpretation may be worse than no interpretation at all.
But even if such pathogens are identified, it remains challenging either to exclude false parasitism (incidental presence in human faeces of eggs resulting from the consumption of an infected animal 7,11 ) or to determine with certainty human outbreaks (helminth eggs might demonstrate their human origin by some circumstantial evidence only 3,11 ). Allometric rules that express parasites and noninfected animals per square meter 12 , in tandem with the several possible contamination pathways, will always lead to diseases with a high global burden 13 . Moreover, a parasitic occurrence can also be related to open water contamination, for instance from livestock grazing in upland areas causing outbreaks downstreams. This has nothing to do with any sanitation structure, as these parasites are by far common and overdispersed 14-16 : hot spots examples of faecal contamination, as shown by highly aggregated Ascaris or Trichuris eggs, are in fact well-known in archaeology and palaeoecology 11,17,18 .
Omitting such a relevant weight of evidence in any comparison between archaeological excavations will introduce de facto a strong bias towards false-positive results into palaeoecological meta-analyses. In the future, to avoid interesting, but geographically misleading or even statistically speculative conclusions, one of the most intriguing hypotheses that will arise might be the investigation by microscopy of soils from archaeological sites associated either with one sanitation infrastructure or without that sanitation. In the case of Roman sanitation, due to the Hadrian's Wall bordering the northern part of the Roman Empire with all its social infrastructures, including latrines, England (entirely inside the Wall during Roman times) and Scotland (outside the Wall during Roman times) can together provide the perfect study area. Again, it seems necessary to emphasize that the Romans created an original system of public sanitation and water distribution on a scale not seen before simply because they linked as first individual hygiene to public health. As it is all too easy to spot patterns in randomly collected data, objective empirical evidence that correlations are real demands a well-designed survey to avoid any suspicion.
There are 2.5 billion people still living on Earth without improved sanitation facilities and an ensured availability of sanitation worldwide is one of the core United Nations targets to end poverty in 2030 (http://www.un.org/sustainabledevelopment/ sustainable-development-goals). Therefore a correct data mining of all nematological records 19 combined with objective interpretation of, probably thin, circumstantial evidence will require great care, as the conclusion shall have implications on ongoing global control programs relating to helminthiases. On the other hand, as the taxonomic status of Ascaris is contentious 20 , palaeoecological evidence from archaeological sites in synergy with present-day molecular ecology can become an unexplored avenue to improve current control programs.

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Version 2 08 August 2017 Referee Report doi:10.5256/f1000research.13196.r24554

Cornelis van Tilburg
Centre for the Arts in Society, Leiden University, Leiden, Netherlands In Mulder's article "Pathogenic helminths in the past: Much ado about nothing", Chelsea Wald and Piers D. Mitchell state that sanitation did not improve people's health significantly, despite its sophisticated technique. In coprolites and remains of toilets throughout the Roman Empire the presence of helminth's eggs of and was widespread, testifying to the unhealthiness of the environment.

Ascaris Trichuris
Mulder states that helminths arrive in the faeces deposit (dung heap or sewer system) through the oral-faecal route; people are infected by eating infected food and drinking infected water, so that there is no immediate connection between sanitation and 'eating' helminth's eggs. Mitchell correctly observes that a concentration of faeces is a breeding-place for parasites and eggs. Faeces was used as a fertilizer in the countryside, so that helminth's eggs were spread.
Comparing ancient sanitation with modern sanitation is not without risk. Mulder's statement 'The large-scale introduction by Romans of fountains into or near public buildings, together with closed aqueducts, can be seen as the very first Water Safety Plan' (second paragraph, 'As a matter … Sea') is disputable. The aqueducts were closed, indeed, but this construction served to prevent pollution (e.g. by pieces of wood) or even poisoning . Moreover, ancient 'safe water' differs from modern 'safe water' .
Nowadays, 'safe water' is water without pollution of by parasites, chemicals, etc. In Antiquity, 'safe water' 1 2 Nowadays, 'safe water' is water without pollution of by parasites, chemicals, etc. In Antiquity, 'safe water' was clear, without smell or taste, like rain and spring water. On the other hand, the aim of the authorities was the same: to improve health and sanitation as much as possible by supplying 'safe water', but the awareness of the Romans was restricted. If necessary, surface water was filtered , but they were unable to remove invisible but noxious elements like helminths' eggs.
In the third paragraph ('Many pathogens … catastrophs') Mulder refers to a tripartite division of waters ('Already… irrigation'), which would be mentioned by Frontinus. I am not aware of any mention of a tripartite division of good, intermediate and bad water in Frontinus; a reference would be welcome. In ch. 11 of , Frontinus describes how the Aqua Alsietina, supplying water of less quality, was De aquis constructed for the Naumachia, a pond for reenacting sea-battles; this aqueduct was not connected with the other aqueducts, being situated on the right bank of the Tiber river. This water was not used, in the first instance, for consumption; surplus of the Naumachia was used for the irrigation of private gardens . In the chapters 88-93, Frontinus criticizes the indiscriminate use of water from aqueducts for any purpose (for instance, the use of clear drinking water for fulleries), and pleads for separating all aqueducts; some aqueducts (like Marcia) containing excellent water have to supply drinking water, other ones (like Anio Vetus) for other purposes .
A small correction in this paragraph: for 'terms' read 'thermae' -which, however, is already covered by 'baths'. I advise to delete this word.