Category Archives: Africa

Yersinia pestis found in human fleas, Madagascar 2013

Madagascar is consistently one of the top two countries in Africa (and usually the world) in cases of plague, caused by Yersinia pestis. For five years prior to January 2013, Madagascar registered 312 to 648 cases per year, with a majority being laboratory confirmed of which >80% were bubonic plague. Of the multiple reservoir species in Madagascar, the black rat (Rattus rattus) is the primary reservoir with Xenopsylla choepus being the main urban vector and Synopsyllus fonquerniei in rural areas.

After a nine case bubonic outbreak in the rural area of Soavina in the district of Ambatofinandrana (shown below), fleas were collected within and outside of five houses over three nights.


The team from the Institut Pasteur de Madagascar collected 319 fleas representing five genera; the most common being the human flea Pulex irritans (73.3%).  In this study, X. cheopis and S. fonquerniei were only collected outside of the houses. Pulex irritans was found only indoors where it made up 95.5% of flea species. Of the 274 fleas tested for Yersinia pestis, 9 pulex irritans were positive. These positive human fleas came from three homes, one of which had a confirmed case of human plague. None of the other flea species tested positive for plague.

Previous observations of pulex irritans in Madagascar suggest this flea may be responsible for domestic human-to-human transmission. High densities of human fleas were reported in plague outbreak villages in 2012-2013. Flea surveys on rats in Madagascar conducted over the last three quarters of a century show that pulex irritans are very rare on rats, suggesting it is not transmitting plague from rats to humans at least in Madagascar. Although pulex irritans are commonly called the human flea, they will feed on dogs and pigs  in addition to humans.  They have also been sporadically found on a variety of other mammals and birds, including rats.

Coping with human fleas as plague vectors will be a significant extra burden on the public health services of Madagascar. Ridding homes of human fleas can be a difficult task. It will however give plague researchers an opportunity to study pulex irritans as a vector in one of the top human plague producing countries in the world.

Within the last ten years, Madagascar has produced human plague cases from three different fleas and pneumonic transmission. With its diversity of plague reservoirs and now flea vectors, Madagascar is illustrating how deeply Yersinia pestis can penetrate and become entrenched in the environment.

Reference:

Ratovonjato J, Rajerison M, Rahelinirina S, Boyer S. “Yersinia pestis in Pulex irritans fleas during plague outbreak, Madagascar” [letter]. Emerging Infectious Disease. 2014 Aug [30 June 2014].http://dx.doi.org/10.3201/eid2008.130629

Wyrwa, J. 2011. “Pulex irritans” (On-line), Animal Diversity Web. Accessed July 01, 2014 at http://animaldiversity.ummz.umich.edu/accounts/Pulex_irritans/

Reactivation of Ancient Plague Foci in Libya, 2009

Landscape around Oran, Algeria,  and Tobruk, Lybia in 2009 that produced plague cases. (Cabanel et al, 2013)
Landscape around Oran, Algeria (2003), and Tobruk, Lybia (2009) that produced plague cases. (Cabanel et al, 2013)

Plague has been called a re-emerging disease primarily because cases have begun to appear in areas where plague has been absent for decades. Two recent surprising outbreaks occurred in Algeria, where plague had been absent for over 50 years, and in Libya after a 25 year absence. A team led by the Institut Pasteur explored possible relationships between the recent Libyan outbreak and the Algerian outbreaks. All of the information in this post comes from their report to be published in the February issue of Emerging Infectious Diseases (citation and link below).

The outbreaks under consideration were just south of Oran, Algeria in 2003, at Lanhouat, Algeria in 2008 and near Tobruk near the Libyan-Egyptian border in 2009. Another possible outbreak of plague occurred at Tobruk during the Libyan revolution in 2011.  Political unrest prevented a complete disease investigation of the 2011 Libyan epidemic. Past Libyan plague outbreaks have occurred from 1913-1920, 1972, 1976, 1977, and 1984. The largest outbreak in 1917 is credited with 1,449 deaths.

The 2009 Libyan index cases consisted of three children from one nomad family; one child died after two days of intensive care and the other two eventually recovered. Only one child had a tender cervical node. The other two, including the child who died, had signs of a severe infection but no visible buboes. The father reported having axillary lymphadenitis and a couple of sudden deaths in the region in the previous two months. A week after admission Libyan authorities reported 13 possible cases to the World Health Organization and requested assistance. The WHO-Libyan team identified two more women with painful inguinal nodes and “infectious syndrome”, but also concluded the initial estimate overstated the number of cases. There are five confirmed cases. The cases were spread 30-60 km from the index family’s home in Eltarsha, 30 km south of Toburk. Regional response included antibiotic treatment of contact persons, and insect and rodent control measures. No further cases were reported.

Diagnosis was confirmed by standard bacteriological assays and molecular characterization. All five confirmed cases were positive with the F1 antigen dipstick.  Yersinia pestis cultures were isolated from three patients,  all phenotyped to the Medievalis biovar by metabolic assays. Molecular characterization confirmed that all are the same Medievalis strain. Hybridization analysis indicates that it is most closely related to, but distinct from, strains isolated from Iranian Kurdistan in 1947 – 1951.

Using the same methods, the 2003 Algerian isolates were phenotyped to the Orientalis biovar. Molecular characterization confirmed that they are all related but not identical Orientalis strains. Activation of multiple related strains from an ancient foci in the same year suggests an environmental trigger. Comparing the 2003 strains to those isolated in 1944 and 1945 illustrate the complexities of plague foci. The 1944 isolate is a Orientalis strain that belongs to the same cluster of strains as the 2003 isolates and other strains from Morocco and Senegal.  The 1945 strain matched a molecular characterization of  Orientalis isolates from Saigon, Vietnam and is believed to have been transmitted by military transports during World War II.  Cabanel et al conclude that the 2003 Algerian outbreaks were caused by local Yersinia pestis strains. It should be noted that the third pandemic from the turn of the 20th century was a Orientalis biovar (1.Ori1).

Cabanel et al. note this is the only instance they could find of a Medievalis strain in Africa. The spread of cases over a 30-60 km region and isolation of related but different strains support the reactivation of an ancient plague focus. Unfortunately they did not have access to isolates from previous 20th century Libyan outbreaks (if they exist) that could have provided more certainty.

Reactivation of plague foci around the Mediterranean has been associated with climate change. They note that an unusually humid winter and good crops in Libya in 2009 favored rodent and flea abundance. Long dormancies may be part of Yersinia pestis’ natural history particularly in resource limited environments. This possibility will be one of the topics of my next post.

Cabanel et al. note that camel meat and livers have been associated with human plague cases in Libya (1976), Saudi Arabia (1994), Jordan (1997), and Afghanistan (2007). Additional local evidence suggested that the highly susceptible camels contracted the plague from local foci in these instances. Although camels do not survive plague long enough to transmit it very far, camel caravan routes may still have played a role in transmission if only by the other organisms also along the camel caravan route. Camels would have provided an abundant host to amplify the organism along the route. Camel fleas could have been carried among the cargo not unlike rat fleas in ship cargoes. Camel caravans would provide an ancient route for a Medievalis strain to reach Libya from the central Asia.

Reference

Cabanel, N., Leclercq, A., Chenal-Francisque, V., Annajar, B., Rajerison, M., Bekkhoucha, S., Bertherat, E., & Carniel, E. (2013). Plague Outbreak in Libya, 2009, Unrelated to Plague in Algeria Emerging Infectious Diseases, 19 (2), 230-236 DOI: 10.3201/eid1902.121031

ResearchBlogging.orgplague series

When Yellow Fever Came to the Americas

“Yellow Jack”, Cornhill Mag., 1892

In the early Americas, nothing scared people more than when Yellow Jack came knocking at the door of their city. Yellow Jack, or as we know it better today Yellow Fever, has rightly been called the plague of the Americas.

It has long been assumed that yellow fever came to the Americas with its vector, Aedes aegypti, in the hold of slave ships. These ships would have been an irresistible feast to the mosquito. Yet, little was known about the origin, locations, and dates of transmission to South America. Juliet Bryant, Edwarld Holmes and Alan Barrett (2007) looked to DNA analysis of yellow fever virus (YFV) strains from 22 countries ( 14 African and 8 South American) to resolve and date the phylogentic tree for YFV. They analyzed 133 isolates from humans and animal hosts collected over a 75 year period.

Bryant, Holmes and Barrett (2007: e75) made four clear observations.

  1. The American strains represent a single clade (monophyletic).
  2. There are two distinct sub-clades in east and west South America respectively.
  3. The South American clade is most similar to the West African isolates.
  4. The East African clade is the most distinctive.

These observations support an east or central African origin for the Yellow Fever Virus dominated by enzootic transmission. Its development parallels the transmission of its vector Aedes aegypti.

The split between the east and west African clades has been calculated to an average distance of 723 years (roughly 1284 AD). The West African isolates are the most diverse in Senegal, suggesting this was an early focus for West African YSF. From West Africa Yellow Fever was transmitted to Brazil a calculated average of 470 years ago (roughly 1537 AD). Early Portuguese seamen frequented this part of Africa and Brazil was their largest colony, founded in 1500. This suggests that Yellow Fever was transmitted to Brazil virtually from the beginning of the Portuguese colony. It is possible that Yellow Fever was one of the imported diseases brought by the Portuguese that decimated native Brazilians before large-scale importation of Africa slaves. The South American clade split into eastern and western populations when it was transmitted to Peru a calculated average of 306 years ago (roughly 1700). There is no evidence of transmission back to Africa or other areas where Aedes aegypti have spread in Asia. Byrant, Holmes and Barrett (2007) argue that sylvatic transmission is the primary means of maintaining YSF in South America. They note that there hasn’t been an urban epidemic of YSF in South America since 1928, unlike the annual urban outbreaks in West Africa.

Auguste et al (2010) confirmed the overall structure of the YSF phylogenetic tree in the Americas, including its Brazilian origin in the Americas. Their analysis of strains collected over the last decade also confirm that Brazil is the reservoir and origin for most strains in the Americas today with the Peruvian strains remaining primarily localized in Peru and neighboring Bolivia. The analysis of Auguste et al (2010) also supports enzootic maintenance and local evolution in areas of spread from Brazil such as Trinidad and Columbia.

What I find most surprising about the YSF tree is its relative youth. This all suggests that Yellow Fever originated in the Middle Ages and probably did not circulate outside of local areas of central Africa until the late medieval period. We still have a lot of learn about the landscape epidemiology of yellow fever including possible vertical transmission among mosquitoes and the importance of difference primate species as reservoirs. Although we have had an effective vaccine for decades, yellow fever is still a very clear and present danger in both the Americas and Africa.

References:

J E Bryant, E C Holmes, & A D T Barrett (2007). Out of Africa: A Molecular Perspective on the Introduction of Yellow Fever Virus into the Americas PLOS Pathogens, 3 (5) : doi:10.1371/journal.ppat.0030075

Auguste, A.J., Lemey, P., Pybus, O.G., Suchard, M.A., Salas, R.A., Adesiyun, A.A., Barrett, A.D., Tesh, R.B., Weaver, S.C. & Carrington, C.V.F. (2010). Yellow Fever Virus Maintenance in Trinidad and Its Dispersal throughout the Americas, Journal of Virology, 84 (19) 9977. DOI: 10.1128/JVI.00588-10