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Permanent Address: http://www.scientificamerican.com/article.cfm?id=sleeping-with-the-enemy
By Kenneth F. Haynes | Thursday, January 19, 2012
Image: Courtesy of Graham Snodgrass/U.S. Army Public Health Command The elderly man lived by himself in a low-income apartment near Cincinnati. But he was not alone. After dark the bed bugs would emerge from his recliner and tattered box-spring mattress to feed on his blood. Judging from the thousands of insects I found in his home, I would venture that it had been this way for many months. Imprisoned by poverty and infirmity, the man had nourished generations of these pests, enduring their bites night after night while their numbers swelled. After largely disappearing for nearly 50 years thanks to the development of DDT and other broad-spectrum pesticides, the bed bug, Cimex lectularius, is making a disturbing comeback—and not just in crowded, urban locales. The bed bug parasite has infested upmarket hotels, college dorms, retail establishments, office buildings, theaters, hospitals, and the homes of rich and poor alike. Though widely dismissed as mere nuisances, bed bugs exact a toll that exceeds the itchy bites they may leave behind: in a 2010 survey of more than 400 individuals living in bed bug–infested dwellings, 31 percent mentioned additional symptoms, ranging from sleeplessness to depression, that they attributed to bed bugs. And a study published in 2011 discovered MRSA bacteria—which cause severe skin lesions—in bed bugs, although much more research will be required to determine whether bed bugs contribute to the spread of MRSA. Bed bugs also cause significant economic losses, as when a hotel has to temporarily close rooms to combat an infestation. One public housing building in Ohio spent about $500,000 on bed bug control, culminating in fumigation of the entire building after more conventional approaches failed to make inroads into the problem. To defeat these unwanted bedfellows, scientists have been endeavoring to figure out how they managed to crawl back into prominence. It appears that bed bugs have benefited from what my University of Kentucky colleague Michael Potter has called “a perfect storm” of factors, including the evolution of insecticide-resistance genes, shifts in control tactics for other urban pests, and changes in patterns of international travel and migration. The good news is that recent studies have suggested novel approaches to detecting incipient populations of the bloodsucking insects before they become full-blown infestations, and these studies have revealed aspects of bed bug biology that might be suitable targets for intervention.
Good Night, Sleep Tight Humanity’s struggle with bed bugs is long-standing. Archaeologists have recovered remains of the parasites dating back 3,500 years to the time of the Egyptian pharaohs. The roots of this relationship go far deeper than that, however. Some experts speculate that the ancestors of bed bugs were parasites of bats. They moved to humans, so the thinking goes, when people took up residence in caves. The relationship between our ancestors and bed bugs became cemented when we shed our nomadic ways in favor of permanent settlements. Still, in temperate latitudes, the onset of winter kept the pests in check. Sensitive to cold, their populations expanded in the warmer months and dwindled in the colder ones. Before the advent of pesticides, our predecessors used every solution imaginable to reduce bed bug numbers, sometimes risking dangers or hardships that modern society would not permit. For example, a 1777 “vermin”-control manual suggested that gunpowder could be ignited in the crevices around the bed (I am not certain if this solution was one of vengeance or practical value). Alternatively, the right species of plants—namely, wormwood and hellebore—boiled with the “proper quantity of urine”—were said to do the job (or did it just force the occupant to seek a different place to sleep?). Arsenic, cyanide and other hazardous compounds were also deployed, with limited success. More commonly, people tackled the problem by intensively cleaning their homes—dousing the permanent parts of the bed with boiling water and kerosene while disposing of the straw mattress ticking. Temporary relief ensued. As central heating of buildings became commonplace in Europe and the U.S., starting in the early 1900s, bed bugs began to flourish year-round. Only with the development of DDT did people finally get real relief from the bugs, starting in the 1940s. First used during World War II to protect U.S. armed forces from mosquitoes and lice, DDT turned out to excel at eliminating bed bugs, too. Its long-lasting efficacy meant that, unlike other treatments on the market, a single application was usually all it took. In a few years the pests had all but disappeared from countries in North America and western Europe and from other developed nations. Unfortunately, DDT and compounds like it also had a part in the near extinction of some predatory birds, among other serious environmental concerns, and they were pulled from store shelves in the U.S. in 1972. Yet even in the absence of DDT, bed bugs did not begin to bounce back until around 2000. Scholars have proposed a number of reasons for this rally. Some have argued that escalating international travel from parts of the world where bed bugs were never under control has allowed the pests to reestablish themselves in areas that had once been cleared of the parasites, although the abruptness of the resurgence does not coincide with any major change in travel frequency. A more influential factor may have been the collapse of political barriers that restricted travel between the East and West, along with increases in the mobility of populations within countries. A shift away from broad-spectrum insecticides other than DDT to much more focused and efficient baits and targeted sprays for roaches, ants and other urban pests could have also allowed bed bugs to slip through the cracks. Even the existence in many communities of affluence alongside poverty may play a role: when a perfectly nice-looking sofa ends up on the sidewalk because it has bed bugs, chances are it will find a home with someone in need. Insecticide resistance has contributed to the problem, too: bed bugs were among the earliest insects to evolve resistance to DDT, with the first cases found in Pearl Harbor just after World War II. (In fact, although some pest controllers advocate for the return of DDT to the bedroom, today’s bed bugs are likely to be resistant to its effects.) And populations the world over have evolved resistance to the insecticides that replaced DDT. Together these forces, combined with the social stigma of bed bugs, which delays effective treatment, can account for the current bed bug pandemic. With a track record of success going back thousands of years, bed bugs are daunting foes. But researchers are gaining on them. One priority is identifying better means of rooting out the insects early on. Because they are small and hide during the day, bed bugs are hard to find and reach. Reliably detecting their presence is key, as is verifying their absence following treatment. One of the simplest detection tools to hit the market recently is the ClimbUp Insect Interceptor, which consists of a shallow bowl with an outer moat (essentially two nested plastic bowls molded into one piece) designed to slip under the leg of a bed. The trap provides information about the source of the bugs: if bugs show up in the inner well, then the bed is a source; if they end up in the outer well, then they must have come from another part of the room. Such a tool might not detect a small population, though, or one that lives behind the headboard. Another new kind of detection device taps into the bugs’ mechanisms for locating human hosts. Traps that incorporate heat and carbon dioxide, along with other undisclosed attractants, are now on the market. A homemade trap made out of an inverted cat dish baited with slowly sublimating carbon dioxide from dry ice is pretty effective, too. As with the double-bowl trap, however, these sometimes fail to reveal bed bugs at the early stages of invasion, when they are easiest to eliminate. At present, nothing beats a well-trained dog when it comes to finding small, dispersed populations of bed bugs. Exactly what the dogs are picking up on remains uncertain, but it might include the bouquet of compounds that researchers at Simon Fraser University identified in 2008 as components of the chemical signals bed bugs use to aggregate. Aside from feeding, everything of consequence to a bed bug—mating, egg laying, development of the immature, and so forth—occurs in hidden harborages that they mark with their own feces, as well as volatile compounds that emanate from the bugs’ bodies. These signals help colony mates find their way back to headquarters. The tendency of bed bugs to gather presumably benefits each individual, perhaps by elevating the humidity in its microhabitat. If we could mimic those aggregation signals, we could develop a simple trap that would allow people to test for the presence of the bugs. Such a trap, if unobtrusive, would no doubt appeal to hotels looking to discreetly monitor guest rooms for bed bugs.
Strange Bedfellows Clearly, we need new ways of eliminating bed bugs once we find them. To that end, scientists around the world have been taking a close look at the unusual mating behavior of these insects in search of possible leads. Bed bug sex is a brutal affair. The males have a saberlike penis that they use to puncture the outer layer, or cuticle, of the female’s abdomen—a form of mating descriptively termed traumatic insemination. The females have adaptations to these damaging copulations. A V-shaped groove in the abdomen called the ectospermalege channels the penetration so that the damage is less costly. Once inside the female’s body cavity, the sperm and any accompanying pathogens encounter a barrier of blood cells loosely organized into an organ with presumed immune function—the mesospermalege. The sperm must migrate through the mesospermalege to a storage area near the base of each ovary. Yet even with these adaptations, my laboratory colonies of bed bugs drift to male predominance because of the injuries caused by multiple copulations. Without human intervention, the colonies would go extinct. In the real world, the bed bugs carry on, probably because females disperse to escape damaging copulations. Why have bed bugs taken off on this costly evolutionary trajectory, whereas females of millions of other insect species have reproductive openings that males use to inseminate them without injury? My colleagues and I are exploring whether this mating behavior is a point of vulnerability. Studies published in 2009 and 2010 by Rickard Ignell of the Swedish University of Agricultural Sciences Alnarp and his colleagues and by Camilla Ryne of Lund University in Sweden, respectively, revealed another intriguing bed bug adaptation to traumatic insemination that could prove useful to humans. Male bed bugs are not very discriminating in their initial sexual encounters. They pounce on other adult males, as well as large immature males and females. Such encounters could lead to life-threatening cuticular damage in these individuals because they lack the adaptations adult females have for sustaining punctures. The researchers found that to deflect these dangerous advances, nymphs and adult males release pheromones that tell the pouncer he is wasting his time and sperm. It does not take much of a leap to imagine manipulating these innate responses to our advantage. In theory, applying synthetic pheromones to bed bug refuges could discourage mating altogether or, if the bed bugs habituate to the odor, could result in costly mating mistakes of the kind that leads to the decline of captive bed bugs. One more aspect of bed bug reproduction warrants mention. As in most sexually reproducing animals, male bed bugs have paired testes that manufacture sperm and a vas deferens that transfers sperm and accessory fluids to the female during copulation, and female bed bugs have ovaries that house eggs and oviducts through which those eggs are released. They also have an organ called the mycetome that contains symbiotic bacteria. When Takema Fukatsu of the National Institute of Advanced Industrial Science and Technology in Japan and his collaborators attempted to figure out what would happen to the viability of bed bugs rendered bacteria-free via antibiotics, they found that females from the bacteria-free colony had lower reproductive rates. Supplementing the females’ blood diet with vitamin B restored their fecundity, indicating that the mycetome bacteria help to provide these nutrients. It is tempting to speculate on the basis of this finding that scientists could treat the host with antibiotics and thus indirectly reach these bacteria, ultimately killing the bed bugs. Yet we need a much more specific solution. Using broad-spectrum antibiotics to treat a person who is not sick could lead to cascading problems. First, the good bacteria in our guts would be displaced, then antibiotic-resistant bacteria would eventually take over, and some of these bacteria would be human pathogens or would lead to our experiencing vitamin deficiencies. The bacteria in the mycetome are a target of opportunity, but we would need to design highly specific antibiotics that hit only these bacteria. As for developing new insecticides, the future is uncertain. Over the past few decades people have relied heavily on insecticides based on compounds called pyrethroids to control bed bugs. Now the bugs are evolving resistance to pyrethroids—no surprise, given that reports of resistance to DDT emerged as early as the late 1940s. DDT and pyrethroids have a common mode of action that often translates into cross-resistance—that is, the development of resistance to one compound affords resistance to the other. My colleagues and I found a population of bed bugs in Cincinnati that was resistant by more than 10,000-fold to a commonly used pyrethroid called deltamethrin, meaning that it takes 10,000 times the dose to kill this strain of bed bugs compared with a naive, susceptible strain. We were startled to see the bugs trudge through a “snowdrift” of nearly pure deltamethrin and still live to feed another day, while their susceptible counterparts perished from exposure to nearly invisible traces of the stuff. They were also cross-resistant to DDT. These Cincinnati die-hards are not unique: my team has detected insecticide-resistance genes in more than 85 percent of the bed bug populations across the country that we sampled. Our lab and others in the U.S. are just starting to identify mechanisms for this resistance. Two of my University of Kentucky colleagues, Fang Zhu and Subba Reddy Palli, have used genetic techniques to restore insecticide susceptibility to resistant strains of bed bugs. Their work suggests enzymes in resistant strains that operate to detoxify insecticides could be targets for human interference. Similarly, my research group has found that a compound well known to enhance insecticide toxicity by targeting that complex of enzymes renders our 10,000-fold-resistant population more susceptible to deltamethrin. The pest-control industry is already using commercial forms of the compound piperonyl butoxide to reinstate some level of bed bug sensitivity to pyrethroids. Researchers may soon be able to quickly identify the mode of resistance in any given bed bug population and then tailor an eradication strategy accordingly, selecting insecticides and synergists that would work on that particular group of pests. Bed bugs are a nightmare, especially for those unable to afford effective countermeasures. Well-trained pest-control operators can conquer infestations with a combination of thorough inspections, knowledgeable use of available insecticides and other tactics, but their efforts are labor-intensive and expensive. For apartment dwellers and home owners, the best bet is to take commonsense measures to avoid bringing bed bugs home in the first place. For my part, when I return from a bed bug–infested apartment, I put my clothes through a cycle in the clothes dryer on the highest setting. Similarly, I might leave my suitcase in a hot car over a sweltering summer weekend rather than risk a home invasion after I travel: sustained exposure to 50 degrees C in every crevice of a suitcase will kill bed bugs. (Freezing bed bugs to death is a more difficult proposition because they can survive many hours of temperatures achieved by household freezers.) It is unlikely that bed bugs will ever return to their recent status as a forgotten pest from our past. But by educating the public about bed bugs and exploring the insects’ unique vulnerabilities, scientists can make inroads. Treating bed bugs as a public health concern and not a social stigma is a step society can take today. |
