Category Archives: mosquitoes

Human Parasites of the Roman Empire

Last week photos of Roman toilets were splashed across the web breaking the news that the Romans were not a healthy as most people seem to have assumed. As with many public health interventions, the real value of a sanitation system is out of view (and out of mind) to most people. Its not the toilet that keeps us healthy; its the water treatment plant. Plumbing just moves waste with its microbes and parasites from one place to another.

Paleoparasitology specialist Piers Mitchell put the Roman public health system to the test by evaluating the evidence for human parasites in archaeological remains from before, during and after the Roman Empire. Comparisons before and after the empire are more difficult in North Africa and the Middle East because these areas had long standing sophisticated civilizations before the Roman empire. There is more clarity between civilizations in Europe since Celtic and Germanic societies did not have anything like Roman infrastructure. Contrary to his expectations, there were just as many parasites and ectoparasites in the Roman era as before or after.  In some cases the empire helped spread parasites across Europe. Relative amounts of parasites across times is difficult to ascertain for a huge variety of reasons. So while the same parasites were present, the degree of infestation would have varied by place and time period, and archaeology can’t reliably predict this.

The Roman achilles’ heel was their use of human waste for fertilizer and fecal contamination of rivers.  Human waste was added to the other manure and redistributed to farm fields and the watershed. What they could not have understood is that human waste is a greater risk for the transmission of human parasites and bacterial diseases. Mitchell also suggests that Roman bath water, that was rarely changed, could have transmitted worm eggs and other parasites. Aquaducts did bring in cleaner water to some of the larger cities but the system could be contaminated and not all Roman sites had access to water from aquaducts. Walter Scheidel (2015:8) has claimed that the city of Rome itself was an example of the”urban graveyard” effect with a very unhealthy population despite having a “heavily subsidized food and water supply”. Scheidel emphasizes the impact of malaria and gastrointestinal disease. We should also keep in mind that a large proportion of gastrointestinal disease would have been bacterial or viral.

Second century Roman mosaic of foodstuffs

As the mosaic to the left shows, the Romans did change agriculture throughout the empire. They spread Mediterranean preferences for cereals and more fish and other aquatic food sources. Mitchell suggests that the Roman love for fish products, especially the fermented fish sauce garum, probably help spread fish tapeworms found throughout the empire. Many parasites and bacterial spores have evolved to withstand preserving methods like smoking, pickling, and osmotic preservation (like salting or sugaring).  Whipworm was the most common parasite found, but round worms and tape worms were also common. Lancet liver flukes were widespread and indicate the (presumably accidental) consumption of ants.  Antibody based detection (ELISA) has been able to identify Entamoeba histolytica that causes the usually endemic amoebic dysentery (as opposed to the epidemic bacterial dysentery caused by Shigella species). Although not strictly speaking parasites, Mitchell notes an abundance of evidence for flies around cesspits suggesting that they contributed to the spread of diseases associated with fecal contamination. He also notes that schistosomiasis has not been identified in Roman Europe, even though it has been found in medieval European remains.

Turning to ectoparasites, Mitchell found ample evidence of head lice, body lice, public lice, human fleas and bed bugs across the Romanized world. Human fleas (pulex irritans) have been particularly well preserved in Roman, Anglo-Scandinavian and medieval York in Britain. Mitchell notes that human fleas and body lice were present in over 50 archaeological layers at York. He concludes that “the Roman habit of washing in public baths does not seem to have decreased their risk of contracting ectoparasites, compared with Viking and Medieval people who did not use public baths in the same way” (Mitchell 2016: 6). Mitchell suggests that there were enough ectoparasites to support particularly lice transmitted diseases. He notes that Plague of Justinian was transmitted by fleas but is non-committal on the likely specific vector.

In examining the impact of the Roman empire, Mitchell notes that the transition from a wide variety of zoonotic parasites to those primarily associated with human fecal contamination had already occurred before the Roman expansion out of Italy. This shift is paralleled elsewhere and is tied to shift from hunter-gathers to settled agriculture. Whipworm, roundworm and amoebic dysentery were the primary parasites of Roman Europe, while the Romans seem to have made a lesser impact on North Africa and the Middle East where endemic zones of parasites were well established.

Malaria is the one parasitic disease I would have liked to see Mitchell discuss more. Mitchell notes that malarial aDNA has been found in Egypt and anemia possibly caused by malaria in Italy. He overlooks all the malaria work by Robert Sallares including malarial aDNA from Late Roman Italy and better anemia studies correlating with malaria have been done in Italy and Britain by Rebecca Gowland’s group. Yet, malaria is such a big topic that it would be hard to cover along with all the other parasites.


Mitchell, P. D. (2016). Human parasites in the Roman World: health consequences of conquering an empire. Parasitology, 1–11.

Scheidel, W. (2015). Death and the City: Ancient Rome and Beyond. Available at SSRN 2609651.

See also:

Hall, A., & Kenward, H. (2015). Sewers, Cesspits, and middens: a survey of the evidence of 2000 years of waste disposal in York, UK. In P. D. Mitchell (Ed.), Sanitation, latrines and intestinal parasites in past populations (pp. 99–120).

Plasmodium knowlesi: A New Ancient Malaria Parasite

There are over a hundred different species of the malaria-causing Plasmodium parasites in reptiles, birds and mammals. Being so widespread among terrestrial vertebrates, zoonotic transfer of Plasmodium has come at humans from multiple different sources. Plasmodium knowlesi had been known for some time as a parasite of long-tailed macaques but was not considered a significant human parasite until 2004 when a large number of human infections were identified in Borneo. Molecular analysis implies that Plasmodium knowlesi is as old as Plasmodium vivax and Plasmodium falciparum.

Cover image the phases of Plasmodium knowlesi from the April 2013 issue of Clinical Microbiology Reviews.

Diagnosis is complicated by the histological similarity between Plasmodium knowlesi and Plasmodium malariae. They can’t be distinguished in blood smears like those shown here, so infections were most often misdiagnosed as P. malariae even though they cause a quotidian (daily) fever. The WHO recommends that microscopic detection in areas where P. knowlesi is found report positive results as “P. malariae/P. knowlesi”.  It can only be securely diagnosed by molecular methods  that can distinguish all five human malarial species. PCR based detection methods have shown promise but no one method has been clinically tested with a large enough number of cases to become the standard of care. Antibody-based Rapid Diagnostic Tests (RDT dipstick tests) for malaria do not reliably detect knowlesi malaria which was discovered in humans after the RDT tests were developed. For now in resource poor areas, microscopic analysis followed by molecular testing where available is the only way to detect knowlesi malaria. Clinical research continues for a RDT test that can be employed areas with poor laboratory resources.

Infections have now been confirmed in all of the countries of southeast Asia. Between 2000 and 2011, 881 cases of local P. knowlesi local transmission have been identified in Borneo, with only 8 cases of P. malariae.  It is now suspected that past diagnoses of P. malariae in the region were actually P. knowlesi. Unlike other forms of malaria, P. knowlesi infects more adults than children, although actual infection rates are still not known.

Long-tailed and pig-tailed macaques are the reservoirs for P. knowlesi. In some areas of Malaysia the macaques are around 90% seropositive for malaria, in one study 87% were P. knowlesi. The malaria vector for P. knowlesi and other malarial parasites is Anopheles leucosphyrus group which is also concentrated in southeastern Asia.  Anopheles balabacensis is the most efficient vector, capable of transmitting P. knowlesi from monkey-to-human, human-to-human and human-to-monkey. A. latens, on the other hand, has been most commonly indicated as the vector to humans in Borneo, where it feeds in the high elevation canopy.  As the map below shows, the macacque reservoir and the mosquito vectors are limited to  the islands and peninsulas south-east Asia. It has been hypothesized, based on genetic diversity, that P. knowlesi has caused human malaria as long as  humans, macaques and the Anopheles vectors have all been on the islands of south-east Asia.

Source: Singh, B., & Daneshvar, C. (2013). Human Infections and Detection of Plasmodium knowlesi. Clinical Microbiology Reviews, 26(2), 165–184. doi:10.1128/CMR.00079-12

Difficulty in diagnosis has made it made it challenging to study the full spectrum of knowlesi malaria across the population. What studies have been done show that it produces a full spectrum of malarial disease from mild to fatal. Most cases reported to-date are in adult males, making an occupational exposure a significant possibility.

Symptoms are representative of other malarial infections: fever, chills and rigor, headache, along with a cough, abdominal pain and diarrhea. Gastrointestinal symptoms correlate with high levels of the parasite in the blood. Thrombocytopenia (low platelet counts) is the most common clinical finding and more severe than in either vivax or falciparum malaria, while anemia appears to be mild in knowlesi malaria. In the few pediatric cases that have been observed, they all responded to anti-malarial therapy. In the few cases of severe disease reported, abdominal symptoms have been so severe in some that malaria was not initially suspected. Acute Respiratory Distress Syndrome (ARDS) has been reported in about 50% of severe cases and acute renal failure in approximately 40%. There have not yet been enough confirmed cases of knowlesi malaria to accurately determine the case fatality rate. Although it appears to respond to a wide range of anti-malarial drugs, an optimized treatment based on a sufficient number of cases was not yet available in 2013.

The discovery of Plasmodium knowlesi in humans comes in the context of increasingly successful control of vivax and falciparum malaria in southeastern Asia. Some of the latest epidemiology from Malaysia suggest that 50-60% of the cases of malaria are now knowlesi. There are fears that knowlesi will jeopardize regional malaria elimination efforts. Is the rate really increasing or is it only apparent as levels of falciparum and vivax decrease? Does a real increase represent an opening niche for knowlesi as vivax and falciparum decrease? Only time and more data will answer our questions.

Primary Reference:

Singh, B., & Daneshvar, C. (2013). Human Infections and Detection of Plasmodium knowlesi. Clinical Microbiology Reviews, 26(2), 165–184. doi:10.1128/CMR.00079-12

For additional epidemiology from Malaysia:

Yusof, R., Lau, Y. L., Mahmud, R., Fong, M. Y., Jelip, J., Ngian, H. U., et al. (2014). High proportion of knowlesi malaria in recent malaria cases in Malaysia, Malaria Journal 13(1), 1–9. doi:10.1186/1475-2875-13-168

William, T., Jelip, J., Menon, J., Anderios, F., Mohammad, R., Mohammad, T. A. A., et al. (2014). Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi, Malaria Journal 13(1), 1–11. doi:10.1186/1475-2875-13-390

The Super-spreading Landscape of Urban Dengue Fever

Dengue Fever is one of the most concerning emerging infectious diseases of the early 21st century. The virus has been spreading with its ever-expanding host, the mosquito Aedes aegypti.  For the last several years there have been naturally acquired cases of dengue fever in the United States and Europe, that are not connected to travel.

Aedes aegypti from Tanzania (Source: Muhammad Mahdi Karim, 2009)

Aedes aegypti‘s preference for the urban environment distinguishes it from most mosquitoes. It prefers to lay it eggs in small urban pools of water – flower pots, old tires, car ruts, buckets – rather than natural forest pools. As day-light feeders, bed netting would not be useful against A. aegpyti.  It has been known for some time that A. aegypti populations are driven by super-producing sites, pools of water that produce the majority of mosquitoes vs. pools that only produce a very few pupae.

It is known that dengue fever is transmitted by super-spreading events but it is unclear how this is tied to A. aegytpi super-production sites and other factors in the environment. To study this phenomena a group of researchers from Yale School of Public Health and the Institiuto National de Salud in Bogota, Columbia chose a dengue fever endemic neighborhood to study the major parameters in transmission. They identified three primary parameters to monitor.

  1. Distribution of super-producing A. aegypti sites across urban plots with similar characteristics. (Mosquitoes generally remain very close to where they hatch and are believed to be exposed to the virus and transmit it within the plot they hatched, or at most a neighboring plot.)
  2. Density of humans domiciled in the plots who can be infected.
  3. Human to mosquito transmission of the Dengue Fever virus. (Humans are the primary reservoir.)

Padmanabha et al devised a new index they call the epidemic potential, secondary infection rate (Ro) per capita.   They hypothesize that human density alters the epidemic potential by altering the dengue viral introduction rate and the secondary infection rate.  Padmanabha et al. note that viral transfer from human to mosquito depends on the number of mosquito bites per person, while viral transmission to humans from mosquitoes depends on the number of different people an infected mosquito bites.

They selected 16 similar urban plots in an endemic neighborhood in Columbia with a range of 41 to 142 homes (1-3 city blocks) with a human density of 3.2 to 4.5 residents per house. They surveyed A. aegypti pupae in water containers to estimate mosquito production and trapped mosquitoes to look for infected adults. Humans immune response to dengue virus was also surveyed over the season. The mosquito surveys were conducted seven times and human immune surveys three times over the season.  They excluded schools, churches and other civil locations were the community gathers from the plots.

Mosquito density results demonstrated super-production sites in each of the seven surveys within each patch. Only 5% of the house surveys accounted for 92% of the total mosquito pupae found. Pupal abundance accounted for nearly 80% of the variation in vector production.  Their model predicted an Ro of 0.88 to 3.87 and correlated with the number of infected humans introductions that produced 20 or more secondary infections; this is only 10% of model repetitions. In most cases introduced viruses to the patch  did not produce secondary infections. Analysis of human-to-mosquito transmission (viral introduction to the patch) and mosquito-to-human transmissions (secondary infections) suggest that both human density and vector abundance alter the dengue Ro and epidemic potential. Models using data generated by this study showed that the intersection of human density and vectors per household produced the best estimates of epidemic potential (Ro per capita). Padmandabha et al noted that “when viral introduction is accounted for, human density amplified the effect of A. aegypti super-production on dengue risk”.  As they monitored the community over the summer with seven surveys they were able to see the decline in super-production decrease the epidemic potential in areas of highest human density.

These super-productive habitats (at the level of individual homes) are seen here to be critical in producing super spreading events of dengue fever. All of the parameters for what makes a super productive habitat including human behavior have not yet been fully explored. This study looked at residential areas with the same socio-economic status. This team is planning further studies that look at a range of socio-economic communities and incorporate community centers like schools and markets.  Studies like this one will be useful for designing strategies to target insecticide programs and other efforts to reduce mosquito abundance and dengue risk.

Padmanabha H, Durham D, Correa F, Diuk-Wasser M, & Galvani A (2012). The Interactive Roles of Aedes aegypti Super-Production and Human Density in Dengue Transmission. PLoS neglected tropical diseases, 6 (8) PMID: 22953017