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The number of cases of Lyme disease reported in the United States has increased from 491 cases in 1982,¹ the first year of national surveillance, to 17,029 in 2001,² despite federal, state, and local efforts to prevent the disease. About 60,000 cases are reported each year in Europe.³ Most efforts at prevention have focused on spreading information about how Lyme disease is transmitted and on encouraging people to use repellents, wear protective clothing, and check themselves for ticks. These strategies are inexpensive and unlikely to be harmful, but their effectiveness has not been conclusively demonstrated. It is possible that these interventions have blunted the increase in Lyme disease in the United States, but they have clearly not been sufficient to lower the number of cases, and the epidemic continues to gain momentum. How can physicians and public health agencies help reduce the incidence of Lyme disease?

The Case for Primary Prevention

Perhaps we should first ask whether primary prevention of Lyme disease is worthwhile. An efficacious and apparently safe vaccine against Lyme disease was withdrawn from the market in February 2002 because of low sales. Of several prevention strategies evaluated in a comprehensive review, vaccination was the only one empirically determined to prevent Lyme disease.⁴ However, demand for the vaccine was apparently dampened by concern about its safety and usefulness. The vaccine was too expensive to be cost saving from the perspective of society.⁵ Optimal protection required multiple and repeated doses.^6,7 There was concern that vaccinated people might abandon other precautions against tick-borne illnesses, thereby increasing their risk of acquiring granulocytic ehrlichiosis and babesiosis. There was a theoretical concern that the vaccine might cause autoimmune arthritis, although this concern was not supported by available data on outcomes.^6,7,8 Sales fell off shortly after the vaccine's introduction, despite intensive marketing.

Does the demise of the Lyme disease vaccine suggest that we should concentrate medical and public health efforts on early diagnosis and treatment instead of primary prevention? Lyme disease is rarely, if ever, fatal and is not contagious. Most people with Lyme disease present early in the infection with a recognizable rash, erythema migrans. About 20 percent of these patients have mild localized infections that will resolve without any treatment, and 90 percent of patients treated for early-stage Lyme disease have an excellent response to antibiotic therapy.^9,10 The most effective antibiotics, amoxicillin and doxycycline, are inexpensive and rarely cause any serious adverse effects.

But Lyme disease is not always a mild illness. Erythema migrans can be accompanied by facial palsy, meningitis, or carditis. The 10 to 20 percent of patients with recognized infection who either do not have erythema migrans or do not notice the rash or seek medical attention for it may present with specific neurologic or joint abnormalities.^{7,10,11,12,13} Although rare, cases of encephalopathy manifested by memory loss, mood changes, and associated neuropathies have been described.¹³ There is one unusual report of a case of Lyme disease in a child that resulted in permanent blindness from ocular nerve damage.¹⁴

Late-stage Lyme disease may require intravenous antibiotic therapy, and about 30 percent of adults with late-stage disease have residual symptoms after treatment.^13,15,16,17 Some of these lingering symptoms may resolve over time, and some may not be directly attributable to Lyme disease; however, the response to treatment is less favorable in the late stage of disease than it is at an earlier stage. Up to 10 percent of patients with Lyme arthritis have persistent joint inflammation, apparently due to an autoimmune arthropathy that is refractory to antimicrobial therapy.¹⁸ A recent randomized clinical trial showed that patients with persistent symptoms after treatment of Lyme disease have substantial impairment in their quality of life but do not benefit from further antibiotic treatment.¹⁹

By recognizing and promptly treating erythema migrans, clinicians can effectively prevent many of the serious late-stage manifestations of Lyme disease. But this strategy may fail to prevent early facial palsy and meningitis, and it will not prevent late-stage manifestations in patients who either do not have or do not detect erythema migrans. Primary-prevention strategies will help reduce these cases, and some strategies may also prevent other tick-borne illnesses, including babesiosis and granulocytic ehrlichiosis in the United States and tick-borne encephalitis in Europe.

Opportunities for Prevention

In North America, Lyme disease is caused by infection with Borrelia burgdorferi (sensu stricto) spirochetes, transmitted to humans by Ixodes scapularis ticks (and, in western areas, I. pacificus). In Europe and Asia, B. afzelii and B. garinii also cause disease in humans. The tick vectors are I. ricinus in Europe and I. persulcatus in Asia. Immature stages of I. scapularis acquire B. burgdorferi primarily by feeding on infected rodents. The infection is passed transtadially from larvae to nymphs, and from nymphs to adult ticks. Adult I. scapularis preferentially feed on white-tailed deer. Humans acquire B. burgdorferi infection when infected ticks (usually nymphs) attach to the skin to feed, but transmission of B. burgdorferi generally requires at least 36 hours of tick attachment.^20,21,22 In Europe, B. afzelii may be transmitted from I. ricinus ticks more rapidly.²³ There are several points in the transmission cycle that provide opportunities to prevent Lyme disease (Figure 1).^7,21,22,24 However, as illustrated by the recent history of the vaccine, no prevention strategy, even if efficacious under experimental conditions, can be effective unless people who are at risk accept it.²⁴

View larger version (38K): [in this window] [in a new window]   Figure 1. Opportunities for Primary Prevention of Lyme Disease during the Transmission Cycle.

 
What should clinicians, public health officials, and residents of communities where Lyme disease is endemic do to prevent the disease? In many parts of Europe and some parts of North America, people can be counseled to avoid tick-infested recreational areas, but this is difficult in the northeastern United States, where ticks infest residential properties.²⁵ Any new vaccine would have to have an extremely reassuring safety profile, be inexpensive, confer long-lasting immunity with only a few doses, and be highly efficacious. It seems unlikely, given the scientific constraints and the less than enthusiastic response to the recent vaccine, that a second-generation vaccine will be marketed in the near future. But there are other primary-prevention strategies that are reasonably likely to be successful (Table 1, Table 2, and Table 3). To prevent Lyme disease at the community level, it is not necessary that all residents adopt the same strategy, but it is necessary that most people adopt at least one strategy.²⁴

View this table: [in this window] [in a new window]   Table 1. Public Health Strategies to Prevent Lyme Disease in Communities.

 

View this table: [in this window] [in a new window]   Table 2. Strategies to Prevent Lyme Disease in the Clinical Setting.

 

View this table: [in this window] [in a new window]   Table 3. Personal-Protection and Residential Strategies to Prevent Lyme Disease.

 
Strategies for Primary Prevention

Tick Checks

Although the effectiveness of tick checks has not been conclusively demonstrated, there is good scientific evidence that removal of an I. scapularis tick within 36 hours after attachment will reduce the risk of B. burgdorferi infection.^20,21,22 Although B. afzelii can be transmitted from I. ricinus ticks more rapidly, the risk of transmission appears to increase with the duration of attachment, so prompt removal of these ticks should also help prevent infection.^23,26 The results of two case–control studies of risk factors for Lyme disease suggested that tick checks might be protective against the disease, although the sample sizes were small and the findings were not statistically significant.^27,28 A population-based, randomized study showed that an educational intervention can increase the proportion of people who check themselves for ticks and use repellents.²⁹ Tick checks can be performed without purchasing any product and appear to be acceptable to residents of areas where Lyme disease is endemic. Surveys in such areas have indicated that less than 54 percent of people tuck their pants into their socks to prevent Lyme disease, 38 to 79 percent use repellents, but 79 to 93 percent check themselves for ticks³⁰ (and unpublished data). If health education programs were to focus on a single personal-protection strategy for community residents, performance of daily tick checks would be the most likely to be accepted and the most likely to be effective. Use of repellents and protective clothing can be recommended on theoretical grounds as supplementary strategies.

Prophylactic Treatment after Tick Bites

Although early studies of the efficacy of prophylactic treatment of tick bites failed to show a significant protective effect, a recent randomized clinical trial showed that a single 200-mg dose of doxycycline administered within 72 hours after a recognized I. scapularis bite had an efficacy of 87 percent (95 percent confidence interval, 25 to 98 percent) in preventing erythema migrans.²² The number needed to treat to prevent 1 case of erythema migrans was 36 among people with any I. scapularis bite and 12 among people with bites from an engorged nymphal I. scapularis. Erythema migrans did not occur in people with bites from unengorged ticks. No serious adverse effects were reported. Nausea or vomiting developed in six people for every case of erythema migrans that was prevented. None of the people treated with antibiotics in this or any of the previous clinical trials had asymptomatic B. burgdorferi infection or any late manifestations of Lyme disease, during follow-up periods that ranged from six weeks to three years.^22,31,32,33

Prophylactic treatment of tick bites would, of course, not prevent Lyme disease among people who do not recognize a tick bite (up to 75 percent of patients with erythema migrans do not notice the tick bite before the rash develops).^34,35,36 The possible effects of prophylactic treatment on other infections transmitted by deer ticks and on strains of borrelia in Europe and Asia, as well as its use to prevent Lyme disease in children, have not been evaluated. Nevertheless, the simplicity, low cost, safety, and high rate of efficacy of a single dose of doxycycline argue for a recommendation of this strategy to prevent Lyme disease among adults who live in areas where Lyme disease is endemic and who seek treatment for a bite from an engorged I. scapularis (Table 2). The risk of nausea and vomiting could be reduced by administering the antibiotic with food. Treatment should be considered if a tick has been attached for 36 to 72 hours but is not needed if the tick has been attached for less than 36 hours. The efficacy of a single prophylactic dose of doxycycline in patients who present more than 72 hours after removing a tick is unknown, and prophylaxis is therefore not recommended under these circumstances.

Clinicians in areas where Lyme disease is endemic should learn to distinguish among the principal tick species in their communities (Figure 2). Although distinguishing among the nymphal stages of ticks can be difficult, Dermacentor variabilis nymphs rarely attach to humans, so in northern areas of the United States where Lyme disease is endemic an attached nymph is most likely I. scapularis. Although Amblyomma americanum nymphs are rarely found in these northern areas, the ticks are found on humans from New York southward — a fact that complicates identification of nymphal ticks in mid-Atlantic coastal regions where Lyme disease is endemic. Bites from D. variabilis and A. americanum do not require prophylactic treatment. Any patient who has been bitten by a tick should be told to seek medical evaluation if signs of tick-borne illness develop.

View larger version (22K): [in this window] [in a new window]   Figure 2. Adult Female Amblyomma americanum (Lone Star Tick), Adult Female and Nymphal Ixodes scapularis (Deer Ticks), and Adult Female Dermacentor variabilis (Dog Tick).

 
Tick Control

Several strategies have been shown to reduce vector-tick populations in areas where Lyme disease is endemic. Tick control to prevent Lyme disease should also reduce the risk of babesiosis and granulocytic ehrlichiosis, which are transmitted by I. scapularis in the eastern United States, and tick-borne encephalitis, which is transmitted by I. ricinus and I. persulcatus in Europe and Asia.^37,38

The most consistently effective method for reducing an abundance of ticks on residential properties is to spray or otherwise broadcast acaricides onto vegetation where the ticks live. A single application of an acaricide such as carbaryl, cyfluthrin, or deltamethrin in early May can reduce populations of I. scapularis nymphs on residential properties by 68 to 100 percent.^39,40,41 Because of the potential toxic effects on organisms that are not targeted, acaricides should be applied as sparingly as possible.⁴² Residents of communities where Lyme disease is endemic and people who apply pesticides should be informed that one well-timed application each year is enough to reduce the number of ticks substantially. In areas where broad application of acaricides is not acceptable, a variety of other tick-control strategies may be useful.

I. scapularis nymphs are frequently found along the edges of forests and spill out onto adjacent vegetation and lawns in suburban settings.²⁵ Since these ticks are extremely susceptible to desiccation, increasing exposure to sun and air by removing brush and leaf litter, or burning foliage, will decrease the number of ticks in the landscaped area.^43,44,45 Laying down wood chips where lawns abut forests can reduce the number of ticks on lawns, presumably by creating a drying barrier between forest and lawn⁴⁶ (and Stafford K: personal communication).

Since adult I. scapularis preferentially feed on deer, tick populations may be decreased in island or peninsular settings by reducing deer populations.^47,48 All or nearly all deer must be removed from an area in order to decrease the number of ticks substantially. Preliminary data from a recent, careful evaluation of this strategy on Monhegan Island in Maine indicate that complete removal of deer resulted in substantial reductions of I. scapularis numbers (Rand P: personal communication). Using fences to keep deer out of residential areas is an effective alternative in some areas where deer removal is not acceptable or practical.⁴⁹

Acaricides can be delivered directly to tick hosts to kill ticks on the animals. In one clever strategy, cotton balls impregnated with permethrin that are placed outdoors are gathered and carried to nests by white-footed mice, the principal reservoir hosts for B. burgdorferi. Ticks on the mice are killed by exposure to permethrin. When tested in Massachusetts, this method completely eliminated I. scapularis nymphs in treated areas.⁵⁰ Unfortunately, when it was tested in Connecticut and New York, there was no decrease in I. scapularis nymphs even after three years of application, indicating that this method may be useful in some ecologic settings but not in others.^51,52

Use of a bait box to attract rodents and directly treat them with the acaricide fipronil, thereby killing ticks on the rodents, was evaluated in a coastal setting in Connecticut (Dolan M: personal communication). Preliminary results indicate that these boxes substantially reduced the number of ticks on treated properties; the device is commercially available under limited circumstances. This strategy requires further evaluation with various methods of acaricide delivery and bait formulations in diverse ecologic settings.

Another baited device to lure deer and treat them with acaricide has the potential to reduce I. scapularis populations over wide areas.⁵³ Preliminary evaluations of the device are promising, but it is not yet commercially available.

Future Techniques for Tick Control

The use of other organisms to control pests has long been part of agricultural pest management. Parasitic wasps, nematodes, and fungi have all been shown to kill I. scapularis.^54,55,56 Some formulations of metarhizium or beauveria fungi have been used against agricultural pests but have not yet been licensed for tick control.

Insecticidal soaps and desiccants are effective in killing I. scapularis in the field.⁵⁷ However, these compounds do not have the residual effects that some of the more broadly toxic acaricides have, so their use must be synchronized carefully with times of maximal tick activity in order to reduce tick populations substantially. Some natural plant extracts have also been shown to kill I. scapularis.⁵⁸ Combining tick pheremones with acaricides may increase the exposure of ticks to the acaricides.⁵⁹ Various birds and ants and other insects eat ticks on occasion, but the logistics of harnessing such predatory relationships to prevent Lyme disease are daunting.

Conclusions

Early diagnosis and treatment of erythema migrans is an important strategy to prevent late stage manifestations of Lyme disease. For primary prevention in Europe and some parts of North America, people can be counseled to avoid areas that are infested with ticks and to remove any attached ticks promptly when a tick-infested habitat cannot be avoided. In areas of the United States where infected ticks infest residential properties, daily tick checks and prophylactic treatment after the detection of engorged I. scapularis ticks should be promoted. In parts of Europe and in communities of the United States where Lyme disease is endemic, strategies to reduce the number of ticks may be effective in decreasing the risk of Lyme disease and other tick-borne illnesses. Methods that are likely to be successful include areawide application of acaricides, landscaping to provide desiccating barriers between tick-infested areas and lawns, and in some settings, exclusion or removal of deer. Host-targeted acaricides and areawide spraying of fungal acaricides show promise but need to be evaluated in various ecologic settings. The strategies most likely to be effective in any given area should be selected on the basis of the local ecology and the preferences of community residents, and they should be evaluated for effectiveness as they are implemented. The cooperative engagement of public health officials, clinicians, and residents of the affected communities will make it possible to reduce the incidence of Lyme disease.

We are indebted to Dr. David Dennis for his critical review of the manuscript; and to Marc Dolan, Dr. Emily Zielinski-Gutierrez, and Dr. Amy Ullman for their help with the illustrations.

Source Information

From the Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, Colo.

Address reprint requests to Dr. Piesman at the Centers for Disease Control and Prevention, P.O. Box 2087, Rampart Rd., Fort Collins, CO 80522, or at jfp2{at}cdc.gov.

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