Canines Contaminated With a Lethal Human Parasite Odor Higher to Insect Vectors | Science

Brazil is home to around 52 million dogs, most of which are popular pets and many of which are home to Leishmania infantum, a parasite that is incredibly harmful to humans. Hundreds of Brazilians die every year when they are bitten by sand flies that got the parasite from dogs. Visceral leishmaniasis, the disease the parasite causes, results in sores on the skin, infections of organs including the spleen and liver, and sometimes death.

A study published today in PLOS Pathogens reports that dogs infected with the parasite may smell more attractive to female sandflies, suggesting that L. infantum could manipulate its hosts on their way from one to the next. Experts say the results could have implications for combating the often fatal tropical disease.

Visceral leishmaniasis is thought to kill between 20,000 and 40,000 people annually, says Christine Petersen, director of the Center for Emerging Infectious Diseases at the University of Iowa, who was not involved in the new study. At least 80 percent of South American cases occur in Brazil, where leishmaniasis has spread since the 1980s and is most likely transmitted by people and their pets as they migrate from rural to urban areas. Brazil’s favelas – overcrowded, low-income urban settlements that are often neglected by authorities – as well as poor areas in India and East Africa are breeding grounds for the disease. “The people who are most at risk of this disease are really in the impoverished parts of the world,” says Petersen.

Gordon Hamilton, a medical entomologist at Lancaster University who co-authored the study, published a study in Scientific Reports in 2017 that found that female sandflies in laboratory settings are more attracted to hamsters infected with L. infantum. About half of the rodents developed an odor that was more attractive to female sand flies. However, hamsters, a model organism that is widely used in laboratory experiments, are not a natural host for the parasite. “It’s more relevant to [study] Dogs with whom the parasite developed together, ”says Hamilton.

In the new study, researchers collected hair and blood samples from 133 infected and healthy dogs in the Brazilian city of Governador Valadares, which is in an industrial area where visceral leishmaniasis is common. The scientists isolated volatile organic chemicals – the molecules that carry scent – from 30 of the hair samples, half of which were from infected dogs, which they then exposed to male and female sandflies in a laboratory. The flies had the choice of approaching the scent molecules of infected or healthy dogs. While the male flies showed little preference between the smells, the females chose the smell of the infected dogs almost twice as often as that of the healthy dogs. “Every single infected dog we tested was more attractive to women than the uninfected dogs,” says Hamilton.

Evidence that female sand flies are more attracted to infected dogs than male flies is important, says Hamilton, as women feed on the blood of dogs and humans and transmit the parasite. Male flies don’t.

“This is the first study to confirm that the smell of infected dogs is significantly more attractive to female sand flies than to male sand flies,” says Filipe Dantas-Torres, a veterinary parasitologist at the Aggeu Magalhães Institute in Recife, Brazil, who was not on the study involved.

Dantas-Torres says that while dogs are the primary hosts of L. infantum, the parasite can infect a wide variety of hosts, including farm animals and cats, which could also act as reservoirs for the disease. Parasites often have a multi-host life cycle – such parasites cause most zoonotic and emerging infectious diseases – and some of them can manipulate their hosts to ensure they are passed on to the next unfortunate victim. Such manipulation can affect the host’s behavior in bizarre ways. For example, the lancet fluke hijacks the ants’ nervous system to ensure that the insects make themselves vulnerable to predators so that they can be eaten. And the Plasmodium parasites that cause malaria make their human hosts smell more attractive to biting insects, which they pass on to the nearest host.

One limitation of the latest study is that the dogs included were mixed breeds. Dantas-Torres says some dog breeds may have attracted more biting insects than others, and the study’s confidence in mutts may have overlooked this. Petersen says it’s also possible the parasite didn’t directly manipulate the dogs odor; infected dogs may smell more attractive to sand flies because, as the disease progresses, the dogs may develop kidney complications that can be malodorous. But Hamilton says infected dogs were significantly more attractive to the female sand flies than uninfected dogs regardless of the parasite load or symptoms observed. Even dogs with a low level of parasite infection still had an odor change that attracted female sand flies.

Both dogs and L. infantum were brought to South America by European colonizers from the Mediterranean region. In Europe, the parasite is transmitted by a species of sand fly that isn’t as effective for a vector as it is in Brazil, but scientists don’t know why, says Hamilton.

Understanding such host-parasite-vector interactions is fundamental to developing more comprehensive approaches to controlling parasites such as Leishmania protozoa, according to Dantas-Torres. Dog infections are largely controlled with topical repellants such as insecticide-laced collars, with vaccinations being a second choice. Petersen says vaccinations could help prevent dogs from contracting the disease that the parasites cause, but they wouldn’t prevent them from carrying L. infantum and potentially passing it on to humans via sand flies. In the hardest-hit areas of Brazil, infected dogs are sometimes killed to control the spread of disease.

According to Hamilton, the results of the new study could open up new avenues of infection control for L. infantum. He is currently involved in a project that uses pheromones to attract sand flies to areas where they can be killed. “If we can figure out what chemicals make infected dogs more attractive, we can possibly combine that with the synthetic pheromone to make it even better,” he says.