Dissemination and salivary delivery of Lyme disease spirochetes in vector ticks (Acari: Ixodidae).
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Biomedical subjects
Publications and source records attributed to A Spielman.
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The seasonal host-seeking pattern of nymphal Ixodes dammini infected with Babesia microti or Borrelia burgdorferi was determined on Nantucket Island, Massachusetts, during 1985. The peak period of host-seeking by infected nymphal I. dammini occurred in May and June. On a per person-hour basis, the number of infected ticks collected reached a maximum in May (Babesia = 17.3; Borrelia = 16.2). The number of infected ticks remained high in June, but decreased notably in July, August, and September. Transmission risk of the tick-borne etiologic agents of Lyme disease and human babesiosis in Massachusetts is greatest during the late spring-early summer months of May and June.
An entomophagous wasp (Hunterellus hookeri Howard) parasitizes about a third of the host-seeking nymphal Ixodes dammini Spielman et al. ticks on Naushon Island in Massachusetts (U.S.A.) where the agents of Lyme disease (Borrelia burgdorferi Johnson et al.) and human babesiosis (Babesia microti Franca) are enzootic. Following blood-feeding, wasp-parasitized ticks are destroyed by the developing wasp. The prevalence of either human pathogen in host-seeking ticks collected in wasp-infested sites is nearly 40% lower than that found in other sites. Nymphal ticks, collected early in their season of activity, are more frequently parasitized by the wasp and less frequently by the Lyme disease spirochaete than those collected later in the summer. Spirochaetes never infected wasp-infected ticks, and few wasp-infected ticks were concurrently infected by the Babesia piroplasm. Taken together, these correlations indicate that the wasp may render the tick inhospitable to both pathogens. The presence of the wasp may have reduced risk of human infection on the island by either pathogen by as much as a third.
Nymphal Ixodes dammini transmitted Borrelia burgdorferi to 1 of 14 rodents exposed for 24 h, 5 of 14 rodents exposed for 48 h, and 13 of 14 rodents exposed for greater than or equal to 72 h. Prompt removal of attached ticks is a prudent public health measure, especially in regions where Lyme disease is endemic.
Permethrin-treated cotton, intended as rodent nesting material, was distributed in wooded sites in which the agents of Lyme disease and babesiosis were enzootic, in order to kill immature Ixodes dammini, the ticks that transmit these human pathogens. Such ticks feed most abundantly on white-footed mice (Peromyscus leucopus), apparently the main reservoir hosts of these agents, and tend to concentrate in mouse burrows. Mice captured after permethrin-treated cotton was distributed, were infested by a tenth as many ticks as were those captured in adjacent nontreated sites, a difference that continued throughout the 4-month period of observation. On average, 72% of all mice captured in treated sites were free of ticks, while virtually all mice captured in nontreated sites were infested. Voles (Microtus pennsylvanicus), however, were tick-infested, regardless of site of capture. Laboratory-reared I. dammini failed to attach to mice captured in treated sites, and most such exposed ticks died. Distribution of permethrin-treated cotton appears to be a means for preventing transmission of the pathogens that cause human babesiosis and Lyme disease.
Brugia malayi microfilariae of specified ages were obtained from gerbils implanted with fertile adult worms. Such microfilariae were tested for their capacity to infect mosquitoes. A strong age dependence was found for the microfilariae's capacity to: penetrate the mosquito midgut, exsheath in response to 20 mM calcium, and develop to third stage larvae in the mosquito. In addition, differences were found between 2-day-old microfilariae and controls (from larva-infected gerbils) in their reactivities with a series of monoclonal antibodies. Thus, defined immunochemical changes occur in microfilariae as they assume functional maturity.
Using the vector tick, Ixodes dammini, we described the reservoir competence of the white-footed mouse, Peromyscus leucopus, for the Lyme disease spirochete, Borrelia burgdorferi. Nymphal I. dammini were used to infect mammals, and larval ticks were used to diagnose infection (a form of xenodiagnosis). One tick was nearly as efficient as more than 1 in transmitting the spirochete to mice. The duration of the prepatent period was about 1 week. Prevalence of infection approached 100% in ticks that fed as larvae on mice infected 2 or 3 weeks previously. Thereafter, infectivity gradually decreased, but duration exceeded 200 days. Hamsters, too, became infectious for larval I. dammini. This report formally demonstrates the life cycle of B. burgdorferi as it seems to occur in nature. We conclude that the white-footed mouse is a competent reservoir for the Lyme disease spirochete.
We investigated whether concurrent ingestion of dengue 2 virus and microfilariae of Brugia malayi would increase viral infection and dissemination rates in Aedes aegypti. Infection rates were similar in mosquitoes that ingested virus alone or both virus and microfilariae concurrently. However, viral dissemination rates, as determined by recovery of dengue virus from both legs and bodies separately, were significantly greater in mosquitoes that ingested both agents concurrently than in those that ingested virus alone. This study confirms that vectorial capacity of a natural vector of an arbovirus may be enhanced by the concurrent ingestion of microfilariae.
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Explore the source record for details and available documents.
Explore the source record for details and available documents.
Lyme disease has recently begun to emerge as a significant threat to human health, both in Europe and the United States. Late sequellae, resembling those of neurosyphilis and multiple sclerosis, may occur many years after initial infection. Spontaneous abortion accompanies arthritis, carditis and neuritis as burdensome short-term sequellae. Thousands of new infections are recognized each year on each side of the Atlantic, although reporting may be incomplete. The disease was described in Europe nearly a century ago and named erythema chronicum migrans, but its etiology has only recently been defined. The name "Lyme disease" was coined to describe a particularly intense American focus of disease, but the term has gained wide acceptance on both continents. The identity of the American and European etiological agents involved has yet to be determined. In America, a deer-associated, often bird-transported tick transmits this mouse-reservoired spirochete. The European situation seems more complex because the vector tick feeds on a greater variety of vertebrates. The reservoir hosts of the spirochete have yet to be determined. The role of Ixodes ricinus and possible other vectors in perpetuating transmission of the European infection remains to be defined. Whether I. ricinus as well as I. dammini merely serve as a bridge to the human population or are important for the maintenance of the feral cycle remains to be seen. The capacity of a tick to maintain transmission of Lyme disease spirochetes depends upon a complex set of properties, including competence as a host for the spirochete, a pattern of feeding that focuses on a particular reservoir favored by a pattern of tick activity, during each transmission season, in which nymphs feed before larvae. Transmission would be favored by an environment, such as that of islands, in which the variety of potential reservoir hosts is restricted. Hosts, for example reptiles, that might fail to support growth of the spirochete would serve to dilute effective transmission in nature. Similarly, the capacity of a vertebrate to maintain the infection requires long-term support of the spirochete in a tissue site accessible to vector ticks, tolerance of repeated feeding by vector ticks and a pattern of host activity that exposes the host to numerous bites. The intensity of infection depends upon a continuous pattern of transmission in which each generation is infected anew. The rare event in which the vector inherits infection would serve mainly to transport the spirochete to a new site, most effectively by migrating birds.(ABSTRACT TRUNCATED AT 400 WORDS)
Saliva of the tick, Ixodes dammini, antagonizes anaphylatoxin, abolishing both the effects of anaphylatoxin on guinea pig ileum preparations regularly stimulated with histamine and the local edema caused by intradermal injection of anaphylatoxin into guinea pigs. Saliva of these ticks, however, did not modify polymorphonuclear leukocyte aggregation induced by anaphylatoxin. Bradykinin and lysil-bradykinin were inactivated, but angiotensin I, angiotensin II, and substance P were not affected. Amino acids were released rapidly following incubation of saliva with bradykinin, but slowly from des-arg-9-bradykinin. These results suggest the presence of a salivary carboxypeptidase with specificity for terminal basic amino acids. Such activity may inactivate anaphylatoxin and bradykinin at the site of tick attachment.
Salivary gland homogenates of adult female Lutzomyia longipalpis inhibited platelet aggregation induced by ADP and collagen. Apyrase (ATP diphosphohydrolase) activity was prominent, requiring Ca2+ but not Mg2+ and a pH optimum of 8.0. Human as well as rabbit hosts developed a well delimited erythema, evident 2-3 min after initial probing and lasting for as long as 2 days. Erythema, not accompanied by itching or swelling, developed in previously exposed hosts as well as in those not previously exposed to this insect. When injected intradermally into the shaved back of a rabbit, salivary gland homogenates induced marked erythema, even with 1/250 of a homogenized salivary gland. This erythema-inducing factor was insoluble in 90% ethanol and was destroyed by incubation with trypsin. These apyrase and erythema-inducing factors, together with short mouthpart stylets, appear to adapt Lutzomyia sandflies to feed on blood released from superficial skin capillaries.
From 1979 to 1983, Lyme disease was studied longitudinally in the 162 long-term residents of Great Island, Massachusetts. In retrospect, the index case occurred in 1962, and the peak years of disease transmission (about three new cases per 100 residents per year) were the late 1970s. Thereafter, during the period of active surveillance, attack rates declined by half. Altogether, 26 (16%) of the 162 residents developed symptoms of the disease. Most of those affected had erythema chronicum migrans, and when untreated, they subsequently developed arthritis or, in one instance, myocarditis. A minority of individuals, mostly children, had arthritis alone. Of 121 asymptomatic residents who gave blood samples, 10 adults (8%) had high titers of IgG antibodies to the Lyme disease spirochete; these titers sometimes persisted for years. From 1981 to 1983, the estimated ratio of apparent-to-inapparent infection was 1:1. The high frequency of Lyme disease on Great Island underscores the need for surveillance and control programs.
Ixodes dammini nymphs were examined for evidence of concurrent infection with Borrelia burgdorferi and Babesia microti. A total of 19 nymphs (18.6%) from Nantucket Island were simultaneously infected, as were 24 nymphs (8.2%) from Naushon Island. These observations are consistent with a common reservoir host for both I. dammini-transmitted pathogens.
To test the possibility that immature deer ticks (Ixodes dammini) may concentrate in the nests of their mouse hosts, we recorded their pattern of detachment. In laboratory experiments, most engorged larvae (greater than 90%) and nymphs (greater than 80%) detached from hamsters between 1200-2000 hours when the 14-hr photophase began at 0600 hours. Time of drop-off was similar regardless of when ticks attached to hosts, but attachment late in the day delayed drop-off by one full day. Ticks detached similarly from naturally-infested Peromyscus leucopus. A post-attachment cue or cues appeared to regulate time of detachment. Such synchronous diurnal detachment may serve to concentrate ticks in the nests of their nocturnal mouse hosts, thereby enhancing pathogen transmission.
Because salivary function and blood location are impaired in sporozoite-infected mosquitoes, we determined whether such pathology also could lead to an increased biting rate. For 5 days, we compared relative daily biting rates of Plasmodium gallinaceum sporozoite-infected mosquitoes (Aedes aegypti) and noninfected mosquitoes with an olfactometer. Mosquitoes then were exposed for 5 min to an anesthetized guinea pig. Infected mosquitoes exhibited a significant increase in olfactometer response which was also reflected in a decreased egg output. We conclude that if duration of contact with a host is limited, then infected mosquitoes may make more attempts at probing before being successful, and thus enhance transmission.