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On river banks

Capivaras and dogs disseminate São Paulo fever in Brazil

FABIO COLOMBINISociable and aquatic: life style facilitates transmission of tick-borne diseasesFABIO COLOMBINI

On one December afternoon, a family of capivaras was resting on the banks of the Pinheiros River, which crosses the city of São Paulo; this river is so polluted that it hardly deserves to be called a river. The capivara family comprised four adults and three capivara babies, separated by a low wall from all the car and trucks on the beltway. The fact that the capivaras were seen there may be the result of an increase in the population of these rodents, the biggest in the world. According to Marcelo Labruna, from the University of São Paulo/USP’s School of Veterinary Medicine and Zootechnology, the capivaras are probably the cause of the resurfacing, in the State of São Paulo, of “maculosa fever,” or “São Paulo fever,” caused by the Rickettsia rickettsii bacteria. In December, this disease killed South African William Charles Erasmus, in Rio de Janeiro; the physicians had been unable to identify the cause of the South African’s fever, headache, muscle pain and exhaustion. The Rickettsia bacteria, which probably infected Erasmus when he was still in South Africa, was only identified through a genetic analysis conducted at the Instituto Oswaldo Cruz after his death. According to Labruna, clinical laboratories in Brazil are not equipped to detect the bacteria; in addition, physicians rarely suspect this disease when they first diagnose the patient.

In Brazil, the Rickettsia rickettsii is the main species and the most aggressive bacteria of this kind that causes São Paulo fever; 40% of the patients infected with this bacteria die. The only reason that this disease has not become a serious public health issue is because it is relatively rare. However, the increase in the number of cases is cause for increasing concern. Reports of the disease in the period from 1920 to 1940 stated that 80% of the patients died in São Paulo and Minas Gerais; three decades went by during which the disease virtually disappeared. Between 1988 and 1997, however, 25 cases were confirmed in six municipal regions of São Paulo State; this number increased tenfold in the period from 1998 and 2007, totaling 255 cases in 54 municipal regions. This growth is partially explained by the fact that since 2001 the State Secretary of Health has required that all diagnosed cases of São Paulo fever be reported to health authorities. In the USP veterinarian’s opinion, however, environmental changes are greatly responsible for the dissemination of the disease. Of these changes, one of the most outstanding are the ones that foster the growth of the capivara (Hydrochoerus hydrochaeris) population. In the 1950’s, the capivara was on the list of endangered species in the State of São Paulo and nowadays it is found in great numbers.

Ticks (Amblyomma cajennense) are the reservoir and vector of this disease. This species of ticks is commonly found in sparsely planted regions, such as the Cerrado tropical savanna region, and forests that line river banks. These ticks commonly attack people in the Southeast region of Brazil. Hundreds of nymphs, the initial stage of the ticks’ life, spread like a cloud of dust throughout the body of the person who is unfortunate enough to touch a leaf full of these insects. The bites cause severe itching, but rarely transmit the disease, although ticks can be born with this disease if the female tick is infected. “We get bitten by ticks every time we go out in the fields, but so far nobody has caught the disease,” says Labruna. The reason is that the host tick is not very susceptible to these bacteria and as infected ticks live and reproduce less, the bacteria only remains in an environment where bigger animals that host it are found.

In an article published in the Annals of the New York Academy of Sciences, Labruna explains the requisites that cause a vertebrate to increase the Rickettsia population: live in the same environment as the bacteria, attract ticks, be susceptible to infection, maintain it long enough to infect ticks and reproduce intensely so that the environment is always populated by animals with no immunity. Capivaras have all these requisites. In collaboration with researchers from the Superintendência de Controle de Endemias/Sucen health authorities, Labruna’s group wrote an article to be published in Veterinary Parasitology journal. In the article, the researchers explain that the infection caused by the São Paulo fever bacteria lasts for approximately ten days. An experiment with four lab-contaminated capivaras showed that during this period the rodents can transmit the bacteria from 20% to 35% of the ticks that feed on their blood, a level of contagion that is much higher than the level observed in other studies.

According to Labruna, the explosion of the capivara population is mostly due to the reforesting of the river banks and the expansion of sugar cane plantations in the state, along with hunting restrictions. “Capivaras seek shelter in the woods, which are also the natural habitat of ticks, and feed on sugar cane,” he explains. As this region does not have predators – wildcats, sucuri snakes, and alligators – it is no wonder that the population density of capivaras living next to the extensive sugar cane fields in the State of São Paulo is 60 times higher than in the Pantanal wetlands region, the capivaras’ natural habitat.

Capivara barbecues, however, are not the most adequate – or legal – solution to control the dissemination of São Paulo fever. “Like other rodents, capivaras reproduce in environments that sustain them,” explains Labruna. Therefore, if someone killed one half of the capivara population, the females would simply bear more babies, which would increase cases of São Paulo fever, because  young capivaras do not have any natural defenses against the bacteria. In the researcher’s opinion, the only immediate way to reduce the disease’s transmission risk would be to limit the capivaras’ access to food, by ,for example, building fences separating the sugar cane fields from the riparian forests, which would prevent access to plentiful food. In addition to keeping the capivara population at bay with less food, limits to their circulation would also reduce the chances of people becoming infected.

In an article available in the Vector-Borne and Zoonotic Diseases site, Labruna wrote that the Didelphis aurita skunk – an animal more commonly found in urban areas, is also a host of this bacteria. His team conducted an experiment in this respect and verified that the skunks remain ill for a longer period of time – three to four weeks – than other species that develop the disease – and infect from 5% to 20% of the ticks during this period.

Marcelo labruna/uspAmblyomma cajennense tick: from small tick, number 1 on the coin to the well-fed formMarcelo labruna/usp

At home
Even if a person never comes near a capivara or a skunk, he can be indirectly infected by these animals if he comes across the tick-borne bacteria. And people don’t even have to go off in the woods for this to happen. “Elderly people who never leave home can catch the disease if they have a dog that goes off into the woods and comes back with ticks,” says Labruna. This is why it is so important to avoid tick infections in dogs, according to an article to be published in Emerging Infectious Diseases, as dogs can also catch São Paulo fever. The symptoms are fever, lack of appetite and exhaustion, the same symptoms as the ones caused by the Ehrlichia canis bacteria, that ticks transmit more frequently to dogs. The two dogs with São Paulo fever, diagnosed at USP, had been taken by a veterinarian from the upscale Jardins neighborhood in São Paulo City to remove the ticks – the dogs had caught the ticks during a trip to the country town of Itu, in the State of São Paulo. When the dogs got the fever, the veterinarian – who had graduated from USP – got suspicious and sent blood samples to Labruna, who is known at the School of Veterinary Medicine as “Marcelo the tick man”. The diagnosis was Rickettsia. “It is possible that this disease is more common in dogs than we suspected,” says the researcher, “and that it is easily confused with Ehrlichiosis, as our laboratories are unable to detect Rickettsia.”

This discovery is even more important, in view of another finding by Labruna: the Amblyomma aureolatum tick, frequently found in dogs, is more susceptible to being infected by Rickettsia than the Amblyomma cajennense tick. In an experiment described in November in the Journal of Medical Entomology, the group from USP stuck small containers full of ticks into guinea pigs infected with São Paulo fever. The group verified that from 10% to 60% of the Amblyomma cajennense ticks contracted the bacteria, and from 80% to 100% of the Amblyomma aureolatum ticks were infected. “In the Metropolitan Region of São Paulo, the Amblyomma aureolatum ticks are greatly responsible for transmitting the disease to human beings.” The situation is not as serious as it seems because these ticks are not very fond of human beings.

In addition, in Brazil, the Rhipicephalus sanguineus tick, also common in dogs, can be on the epidemiology map of São Paulo fever. The risk seems to be serious, because the life cycle of these ticks is closer to that of human beings: they spend their entire lives on dogs and, when they are released, they can show up in homes, walking around the walls and fences. The results are described in the Vector-Borne and Zoonotic Diseases site. In 2005, the group collected 481 ticks from dogs living in the Recreio da Borda do Campo community in Santo André, located in São Paulo’s Metropolitan Region, and verified that 1.3% of these dogs were infected with R. rickettsii, the same level of infection that other studies had found in relation to the Amblyomma cajennense ticks.

The veterinarians from USP have also expanded the search for other agents of the disease. The Rickettsia parkeri bacteria, for example, causes a milder version of São Paulo fever, and this can make accurate diagnosis difficult. Through genetic analyses, the USP veterinarians recently discovered another species of the Rickettsia, which they presented at the International Conference on Ticks and Tick-Transmitted Pathogens held in Argentina in September. The name of this species is Rickettsia monteiroi, named in honor of José Lemos Monteiro, a researcher from the Instituto Butantan, who died from São Paulo fever in 1935, while working on a vaccine for this disease. In the last ten years, reports on the disease have come from all the Southeastern states. A milder form of São Paulo fever, which does not lead to death, seems to have appeared in the State of Santa Catarina – it is probably another species of Rickettsia. In Labruna’s opinion, it is necessary to understand the ecology of the bacteria more thoroughly, in order to deal with the disease. In the meantime, the solution is to remove ticks after walking in the country and spray dogs with anti-tick lotions.

The Project
The evaluation of the role of capivaras, skunks and pet dogs in the epidemiology of Brazilian São Paulo fever (nº 06/50918-0); Type: Regular Research Awards; Coordinator: Marcelo Bahia Labruna – FMVZ-USP; Investment: R$ 135,809.00 (FAPESP)

Scientific Articles
LABRUNA, M.B. Ecology of Rickettsia in South America. Annals of the New York Academy of Sciences. Forthcoming.
SOUZA, C.E. et al. Experimental infection of capivaras by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Veterinary Parasitology. Forthcoming.
Vector-Borne and Zoonotic Diseases: