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Do Tick Attachment Times Vary between Different Tick-Pathogen Systems?

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Improvements to risk assessments are needed to enhance our understanding of tick-borne disease epidemiology. We review tick vectors and duration of tick attachment required for pathogen transmission for the following pathogens/toxins and diseases: (1) Anaplasma phagocytophilum (anaplasmosis); (2) Babesia microti (babesiosis); (3) Borrelia burgdorferi (Lyme disease); (4) Southern tick-associated rash illness; (5) Borrelia hermsii (tick-borne relapsing fever); (6) Borrelia parkeri (tick-borne relapsing fever); (7) Borrelia turicatae (tick-borne relapsing fever); (8) Borrelia mayonii; (9) Borrelia miyamotoi; (10) Coxiella burnetii (Query fever); (11) Ehrlichia chaffeensis (ehrlichiosis); (12) Ehrlichia ewingii (ehrlichiosis); (13) Ehrlichia muris; (14) Francisella tularensis (tularemia); (15) Rickettsia 364D; (16) Rickettsia montanensis; (17) Rickettsia parkeri (American boutonneuse fever, American tick bite fever); (18) Rickettsia ricketsii (Rocky Mountain spotted fever); (19) Colorado tick fever virus (Colorado tick fever); (20) Heartland virus; (21) Powassan virus (Powassan disease); (22) tick paralysis neurotoxin; and (23) Galactose-α-1,3-galactose (Mammalian Meat Allergy-alpha-gal syndrome). Published studies for 12 of the 23 pathogens/diseases showed tick attachment times. Reported tick attachment times varied (<1 h to seven days) between pathogen/toxin type and tick vector. Not all studies were designed to detect the duration of attachment required for transmission. Knowledge of this important aspect of vector competence is lacking and impairs risk assessment for some tick-borne pathogens.
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environments
Review
Do Tick Attachment Times Vary between Different
Tick-Pathogen Systems?
Stephanie L. Richards 1, *, Ricky Langley 2, Charles S. Apperson 3and Elizabeth Watson 4
1Department of Health Education and Promotion, Environmental Health Science Program,
East Carolina University, Greenville, NC 27858, USA
2Toxicology Program, North Carolina State University, Raleigh, NC 27695, USA; rick.langley@dhhs.nc.gov
3
Department of Entomology, North Carolina State University, Raleigh, NC 27695, USA; apperson@ncsu.edu
4Animal Hospital of Boone, Boone, NC 28607, USA; lizwatson489@gmail.com
*Correspondence: richardss@ecu.edu; Tel.: +252-328-2526
Academic Editor: Andrea Cattaneo
Received: 30 March 2017; Accepted: 4 May 2017; Published: 9 May 2017
Abstract:
Improvements to risk assessments are needed to enhance our understanding of tick-borne
disease epidemiology. We review tick vectors and duration of tick attachment required for pathogen
transmission for the following pathogens/toxins and diseases: (1) Anaplasma phagocytophilum
(anaplasmosis); (2) Babesia microti (babesiosis); (3) Borrelia burgdorferi (Lyme disease); (4) Southern
tick-associated rash illness; (5) Borrelia hermsii (tick-borne relapsing fever); (6) Borrelia parkeri
(tick-borne relapsing fever); (7) Borrelia turicatae (tick-borne relapsing fever); (8) Borrelia mayonii;
(9) Borrelia miyamotoi; (10) Coxiella burnetii (Query fever); (11) Ehrlichia chaffeensis (ehrlichiosis);
(12) Ehrlichia ewingii (ehrlichiosis); (13) Ehrlichia muris; (14) Francisella tularensis (tularemia);
(15) Rickettsia 364D; (16) Rickettsia montanensis; (17) Rickettsia parkeri (American boutonneuse fever,
American tick bite fever); (18) Rickettsia ricketsii (Rocky Mountain spotted fever); (19) Colorado
tick fever virus (Colorado tick fever); (20) Heartland virus; (21) Powassan virus (Powassan disease);
(22) tick paralysis neurotoxin; and (23) Galactose-
α
-1,3-galactose (Mammalian Meat Allergy-alpha-gal
syndrome). Published studies for 12 of the 23 pathogens/diseases showed tick attachment times.
Reported tick attachment times varied (<1 h to seven days) between pathogen/toxin type and tick
vector. Not all studies were designed to detect the duration of attachment required for transmission.
Knowledge of this important aspect of vector competence is lacking and impairs risk assessment for
some tick-borne pathogens.
Keywords: duration of tick attachment; tick-borne disease; tick; transmission dynamics
1. Introduction
Ticks (Class Arachnida; Order Acari) are widespread across the United States (US) and tens
of thousands of tick-borne diseases are reported yearly in the US. Approximately 40 tick species
blood feed on humans in the US [
1
] and at least 11 of these species are known to transmit infectious
agents [
2
4
]. The Centers for Disease Control and Prevention recognizes the following tick-borne
diseases and pathogens in the US: Anaplasmosis, babesiosis, Borrelia miyamotoi disease, Colorado tick
fever, ehrlichiosis, Heartland virus, Lyme disease, Powassan disease, Rickettsia parkeri rickettsiosis,
Rocky Mountain spotted fever, tick-borne relapsing fever, tick paralysis, tularemia, Q-fever, and 364D
rickettsiosis [4].
Numerous studies have documented tick exposure as an occupational health issue for forestry
personnel and others working (e.g., agricultural industry, military) and/or participating in recreational
activities (e.g., hunting, hiking) where tick exposure is common. A study in Germany showed evidence
for previous infection of foresters for tick borne pathogens Bartonella Strong, Borrelia burgdorferi Johnson,
Environments 2017,4, 37; doi:10.3390/environments4020037 www.mdpi.com/journal/environments
Environments 2017,4, 37 2 of 14
Coxiella burnetii Derrick, Francisella tularensis McCoy and Chapin, and tick-borne encephalitis virus [
5
].
The same study reported a high incidence (31%) of Borrelia burgdorferi (the causative agent of Lyme
disease) seropositivity in participants was related to these characteristics: (1) male; (2)
50 years
old; (3) reported >50 tick bites; and (4) worked in the forest. A study in Poland also found high
incidence (50%) of Borrelia burgdorferi antibodies in forestry workers [
6
]. A study in US National
Park Service employees showed prior infections with tick-borne pathogens, such as Bartonella henselae
Regnery, spotted fever group rickettsiae, and Anaplasma phagocytophilum Foggie [
7
]. However, most
studies, including the aforementioned studies, do not ask participants about how long ticks were
attached before being discovered/removed. In order to develop strategies to prevent occupational
and recreational exposure to ticks and tick-borne diseases, we must have improved knowledge and
education of risk factors [
5
]. This includes health education about the importance of removing ticks as
quickly as possible to reduce the chance of pathogen exposure. A study in military personnel showed
that health education increased self-awareness and removal of ticks and this reduced tick bites [
8
].
Military personnel may be exposed to tick-infested areas for multiple days (unlike foresters and/or
recreational exposure), hence, removal of ticks while in the field is essential to reduce attachment
times that can lead to pathogen transmission by infectious ticks. Individuals can also use preventative
measures, such as wearing permethrin-treated clothing and/or repellant, in order to minimize tick
exposure risk. Studies have shown these types of practices can reduce the incidence of tick bites, hence,
reducing the potential for pathogen exposure [9,10].
Pathogen transmission by ticks depends on a variety of factors including duration of feeding time,
pathogen titer, and extent of tissue (e.g., gut, salivary glands) infection at the time of blood feeding.
Some pathogens require a period of replication and/or expansion
(in response to a blood meal)
prior to transmission from a tick. Consequently, host infection may be prevented if the tick is
removed within a critical period of time after attachment; i.e., the longer a tick remains attached,
the higher the likelihood that an infectious pathogen dose is transmitted [
11
13
]. Replication and/or
expansion has been documented for bacterial pathogens causing Rocky Mountain spotted fever,
anaplasmosis, Lyme disease, and babesiosis [
14
]. Tick-borne viruses differ from bacteria in the
duration of replication/expansion required (if any) and may be transmitted more rapidly than
bacteria [
12
,
14
]. It is important to note that not all ticks can become infected with, and transmit,
all pathogens. Non-competent ticks may be able to acquire a pathogen from a host during blood
feeding, but may not be able to sustain the pathogen through molting, and/or be able to transmit the
pathogen. Immune responses to pathogens may be greater in non-vector competent ticks compared to
ticks that are competent vectors [15,16].
Our findings indicate that the duration of tick attachment to vertebrates required for transmission
of pathogens (e.g., bacteria, viruses) varies, with most information derived from experimental studies
conducted on rodents e.g., [
14
,
17
]. The few studies of humans have largely been clinical investigations
of disease case patients, e.g., [
18
,
19
]. Engorgement indices (the ratio between total tick body length
and scutum length (or width); the ratio between alloscutum width and scutum width) were calculated
to determine the duration of feeding for Ixodes scapularis Say [
20
]. It is unknown whether these indices
can be applied equally to all tick species. After 24 h of attachment to laboratory rabbits, engorgement
indices increased steadily in I. scapularis when assayed at 36, 48, and 60 h post-attachment [
20
]. The total
tick body length and alloscutal width increased with increased blood feeding attachment time, while
scutal length and width remained the same. The same study showed that, based on the engorgement
indices, most (64%) adult ticks submitted for pathogen testing (for a variety of pathogens, such as
Borrelia burgdorferi) by human bite victims had been attached for
36 h, while only 41% of nymphs
were removed at the same time point.
Hard ticks (Arachnida: Acari: Ixodidae) can mate on (usually Metastriata) or off (usually Prostriata)
the host [
21
]. After attachment, the mated female hard tick will engorge to ca. 100–200 times her unfed
weight (depending on tick species) in order to develop eggs and subsequently oviposit [
15
,
22
]. A virgin
female tick usually feeds only until the critical weight (10 times her unfed weight) is achieved and
Environments 2017,4, 37 3 of 14
may wait on a host until a male finds her and copulation takes place [
22
]. If a virgin tick is removed
prior to mating, she may continue blood feeding at a later time if she has not yet reached the critical
weight [
22
]. Once attached to a vertebrate host, a mated female hard tick feeds for four to 15 days
to acquire enough blood to develop eggs [
22
,
23
]. There is an initial slow feeding phase (
7 days in
adults) where the hard tick increases in size by ca. 10 times (critical weight) (in virgin and mated
females), followed by a rapid feeding phase (12–24 h) (in mated females only) [
22
,
23
]. Others have
shown that the mating stimulus for the rapid feeding phase in females may be something the male
inserts via spermatophore, but not necessarily sperm, as irradiated male sperm (sterile) have still been
shown to stimulate rapid feeding in Dermacentor variabilis Say [
24
]. The virgin female tick does not
feed to a level above the critical weight so she can (1) remain small and reduce the chances of being
detected (and potentially removed by grooming) by the host, or (2) have the opportunity to reattach to
another host to find a mate, if needed [22].
Hard ticks secrete an adhesive “cement” composed of proteins during the first five to 30 min of
attachment (during the slow feeding phase) that helps secure them to the host [
23
,
25
,
26
]. Over time,
additional layers of cement are secreted [
27
]. Studies on tick-borne encephalitis virus have shown higher
virus titers in the cement plug than in the tick body (e.g., Ixodes ricinus (L.), Ixodes persulcatus Schulze),
hence, even after a tick is removed, disease-causing pathogens may still be present in the host [
26
].
Mouthparts of different tick genera differ in length (e.g., shorter mouthparts extending into the dermis
and epidermis for Dermacentor,Haemophysalis, and Rhipicephalus, compared to longer mouthparts
extending more deeply into the dermis for Amblyomma and Ixodes) [
15
]. The amount of pathogens in
the mouthparts of the tick would be expected to vary between vector-pathogen systems, hence, leaving
remnants of tick mouthparts in the body after removal may leave pathogens behind, and possibly result
in secondary infection [
28
]. However, if the tick and tissue surrounding the tick bite site are removed
before pathogens (e.g., spirochetes) have had time to disperse, infection may be prevented [29].
Soft ticks (Arachnida: Acari: Argasidae) mate off the host, tend to inhabit animal burrows,
and require a shorter feeding time (ca. 30–60 min) to fully engorge than hard ticks [
15
]. The weight
of a blood-fed female soft tick is ca. five to 12 times her unfed weight [
30
] and, unlike hard ticks,
mating status does not influence the blood meal size [
22
]. Based on documented differences in
engorgement periods, pathogen transmission by soft ticks may occur more rapidly than via hard ticks.
Others have shown a dose-dependent relationship for successful pathogen transmission demonstrated
by simultaneous blood feeding by multiple soft ticks (e.g., three Ornithodoros turicata Duges start
transmitting Borrelia turicatae to mice within 15–40 s (tick-borne relapsing fever)) [31].
Here, we review some important pathogens of public health concern transmitted by hard and soft
ticks and associated diseases with a focus on the US. For each disease, we investigated the known tick
vectors and (if known), and the duration of tick attachment required for pathogen transmission.
2. Materials and Methods
We used worldwide literature retrieval databases: PubMed, Web of Science, Armed Forces Pest
Management Board Literature Retrieval System, and Google Scholar. Terms used in the literature search
included: “duration of tick attachment and tick-borne diseases”, “transmission dynamics of tick-borne
diseases”, “anaplasmosis”, “ehrlichiosis”, “Rocky Mountain spotted fever”, “Rickettsia parkeri”,
“tularemia”, “Colorado tick fever”, “Powassan disease”, “babesiosis”, “Lyme disease”, “Southern
tick-associated rash illness”, “tick-borne relapsing fever”, “Borrelia miyamotoi”, “Heartland virus”,
“364D rickettsiosis”, “tick paralysis”, “occupational health tick exposure”, and “tick meat allergy”.
Literature searches were conducted between January 2014 and April 2017. Reference sections of
primary articles were also reviewed for related publications.
3. Results
A summary of associated tick vectors and the duration of tick attachment time for transmission
(if known) are listed in Table 1.
Environments 2017,4, 37 4 of 14
Table 1. Summary of attachment times reported in publications. Primary known US vector(s) are indicated in bold.
Pathogen(s) Associated Disease Arthropod Epidemiologic Vectors in US Estimated Duration of Attachment
Time to Transmit Pathogen
References for Attachment Time
(Time Points Examined-Host)
Anaplasma phagocytophilum Anaplasmosis I. scapularis *, I. pacificus 24 h–50 h
[32] (24, 48, 72 h-C3H/HeJ and
C3H/Smn.CIcrHSD mice);
[33] (12, 24, 30, 36, 50 h-C3H/HeJ mice)
Babesia microti Babesiosis I. scapularis * 7–18 days
36–54 h
[34] (every 24 h from 6–25 days-voles);
[34] (36, 48, 54 h-hamsters)
Borrelia burgdorferi Lyme disease I. scapularis *, I. pacificus * 4–72 h (Ixodes scapularis);
48–96 h (Ixodes pacificus)
[17] (24, 48, 72, 96 h-deer mice);
[35] (24, 48, 72 h, 96 h-mice);
[36] (24, 48, 60, 72, 96, 192 h-only salivary
glands tested [no host transmission];
[37] (4, 12 h-human clinical case report)
Borrelia lonestari **, possibly other Borrelia spp.
Master’s disease, Southern tick associated rash illness
A. americanum * Unknown n/a
Borrelia turicatae, Borrelia hermsii Tick-borne relapsing fever O. hermsii *, O. turicata *, O. parkeri
15 s–30 min
(transmission related to [rapid] time for
engorgement in soft ticks)
[38] (6–23 min-unknown host;
[31] (15 s, 30 min-Swiss Webster mice)
Borrelia hermsii, Borrelia parkeri Tick-borne relapsing fever O. hermsii *, O. turicata *, O. parkeri Unknown n/a
Borrelia mayonii Borreliosis **** I. scapularis * 24–96 h [39] (24, 48, 72, 96 h-CD-1 mice)
Borrelia miyamotoi Borrelia miyamotoi disease (Borreliosis) **** I. pacificus *, I. scapularis * 24–96 h [40] (24, 48, 72, 73-96 h-mice)
Coxiella burnetii Query Fever
A. americanum, A. cajennense, D. andersoni *,
D. occidentalis, O. coriaceus Koch, O. hermsi
(primary epidemic vector unknown)
Unknown n/a
Ehrlichia chafeensis, Ehrlichia ewingii Ehrlichiosis A. americanum, D. variabilis 24–50 h
(A. phagocytophila)
[33] (12, 24, 30, 36, 50 h-C3H/HeJ mice);
[35] (24, 48, 72-mice)
Ehrlichia muris n/a I. scapularis Unknown n/a
Francisella tularensis Tularemia
A. americanum, D. andersoni,
D. variabilis *
(also transmitted via aerosolized
contact with or ingestion of infected animals)
48 h [41] (48, 96, 144 h-saliva collected in
capillary tube)
Rickettsia 364D n/a D. occidentalis Unknown n/a
Rickettsia montanensis n/a D. variabilis Unknown n/a
Rickettsia parkeri
Tidewater spotted fever, American boutonneuse fever,
Maculatum rickettsiosis A. maculatum *** Unknown n/a
Rickettsia rickettsii Rocky Mountain spotted fever D. variabilis, D. andersoni, Rh. sanguineus 2–96 h [42] (2 h increments from 2–18, 24, 36, 48,
>96 h-guinea pigs, rabbits)
Colorado tick fever virus Colorado tick fever, mountain fever D. andersoni Unknown n/a
Heartland virus n/a A. americanum Unknown [43] (unknown attachment time-rabbits)
Powassan virus Powassan disease D. variabilis, D. andersoni, I. scapularis * 15–30 min [14] (15, 30, 60, 180 min-BALB/c mice)
Neurotoxin (possibly ixovotoxin) Tick paralysis
A. americanum, A. maculatum, D. andersoni,
D. variabilis, I. pacificus
(primary epidemic vector unknown)
5–7 days [18] (human clinical case reports)
carbohydrate galactose-α-1,3-galactose Meat allergies (alpha-gal syndrome) A. americanum Unknown n/a
* Transmission capacity verified in laboratory animals; ** Pathogen not observed in all cases; *** A. maculatum did not become infected after feeding on cotton rats in the laboratory
study [44]; **** Similar to Lyme disease.
Environments 2017,4, 37 5 of 14
3.1. Anaplasma phagocytophilum (Anaplasmosis)
Anaplasmosis is caused by an intracellular bacterium infecting white blood cells.
Anaplasma phagocytophilum (previously Ehrlichia phagocytophilum) is primarily transmitted by I. scapularis
and Ixodes pacificus Cooley and Kohls. Transmission dynamics for anaplasmosis are not as well studied
as are those for Lyme disease [
35
]. Anaplasma phagocytophilum inhabit the salivary glands of ticks
more frequently than the midgut. One study exposed mice to nymphal I. scapularis infected with the
NTN-1 strain of granulocytic ehrlichiae E. phagocytophilia (now A. phagocytophilum) [
33
], although the
dose of pathogen imbibed by the ticks was not reported. Once ticks molted after blood feeding, they
were held for two months prior to feeding on naïve mice. One of the 11 mice became infected with
A. phagocytophilum after 24 h of tick attachment, zero of five at 30 h of attachment, eight of 12 at 36 h
of attachment, and 11 of 13 after 50 h of attachment [
33
]. Another study assessed eight mice exposed
to the NCH-1 strain of A. phagocytophilum-infected I. scapularis nymphs for 40 h (four mice) and 48 h
(four mice) [
32
]. The same study showed that no mice exposed to ticks for 40 h were infected, while
100% of mice exposed for 48 h were infected with A. phagocytophilum [
32
], indicating that replication
of A. phagocytophilum may be required for efficient transmission. The same study gave details about
the pathogen dose imbibed by ticks. It is also unknown how long molted ticks were held prior to
feeding on naïve mice for the transmission study. The two studies shown here [
32
,
33
] may have used
different doses of the granulocytic agent to infect ticks (although these details are unclear) and this
could have impacted the infection titer of the ticks that were used, hence, impacting the duration of
tick attachment time required for transmission. Regardless, together both studies indicate that at least
24 h are required for transmission and transmission was increased dramatically after 48–50 h. It is also
possible for this pathogen to be transmitted transovarially [45].
3.2. Babesia microti (Babesiosis)
Babesia microti Babes is an apicomplexan protozoan parasite that causes babesiosis in
vertebrates [
34
]. After an uninfected tick imbibes a Babesia-infected blood meal, ookinetes eventually
escape the midgut into other tissues, where kinetes develop and invade the salivary glands [
46
].
An infectious tick vector transmits Babesia spp. sporozoites to vertebrate hosts and this pathogen
can also be transmitted transstadially and transovarially in ticks [
46
]. This pathogen is primarily
transmitted by I. scapularis [47].
Ticks feeding on mice co-infected with B. microti and B. burgdorferi were twice as likely to become
infected with B. burgdorferi compared to B. microti; however, the study did not assess subsequent pathogen
transmission rates [
48
]. Ticks were tested for pathogens up to six weeks after molting [
48
]. Babesia microti
was transmitted to hamsters when I. scapularis was attached for
36 h [
37
]. The same study showed that
9% of hamsters were infected after 36 h of attachment, 17% infected after 48 h, and 50% infected after
a period of 54 h of attachment (mean
±
standard deviation; 9.5
±
4.3 ticks/hamster). It is possible that
the number of infected ticks infesting a vertebrate host and, hence, the number of parasites potentially
invading that host, would complicate this analysis of duration of attachment time. Ideally, in a study to
determine the duration of the attachment time required for transmission, each replicate would include
examining the time it takes for one infected tick (with a known pathogen titer) to infect one naïve
vertebrate host.
3.3. Borrelia burgdorferi (Lyme Disease)
Borrelia burgdorferi is transmitted by I. scapularis and I. pacificus [
49
]. Nymphal and adult ticks
may transmit the pathogen to humans; however, I. scapularis nymphs are the most significant life
stage involved in transmission because of their small size and spring-summer activity pattern [
49
].
Much attention has been paid to the time of tick attachment required to transmit B. burgdorferi and it is
estimated that 300,000 human cases/year occur in the US [
50
]. Tick larvae or nymphs become infected
after feeding on a spirochaetemic vertebrate reservoir host [
50
]. After ticks molt to the next life stage,
Environments 2017,4, 37 6 of 14
spirochetes reside in the tick midgut and must disseminate to the salivary glands for transmission
during feeding [
35
,
36
]. The number of spirochetes was examined in the midgut and salivary glands of
I. scapularis nymphs during attachment to mice [
36
]. The mean numbers of B. burgdorferi spirochetes
in infected tick midguts increased six-fold from pre-feeding to 48 h post-attachment [
36
]. For ticks
that already had infected salivary glands, the mean number of spirochetes/pair of salivary glands
rose by five-fold at 24 h and 21-fold at 72 h [
36
]. The same studies showed that the fastest increase in
spirochete replication in the salivary glands occurred during 48–60 h post-attachment. These findings
are consistent with laboratory animal studies where B. burgdorferi was rarely transmitted during the
first 24 h of tick attachment [
45
]. Similarly, another study showed the transmission rate of B. burgdorferi
to hamsters via I. scapularis increased over time (i.e., 24 h (7%), 48 h (36%),
72 h (93%)) [
51
]. To our
knowledge, it is not possible for B. burgdorferi to be transmitted in ticks transovarially [52].
A study in New York State investigated tick attachment times (estimated by scutal index) in
patients and examined incidence of erythema migrans (EM) and Lyme disease serology [
53
]. The odds
of developing EM or seroconversion were 23 times higher for patients having a nymph or adult female
I. scapularis attachment lasting
72 h compared to those with <72 h of attachment. A relationship
between the scutal index and patient reports of attachment time was only demonstrated in 49%
of patients [
53
]. Studies using human tick bite patients highlight the difficulty of estimating tick
attachment time versus risk of pathogen transmission. Patients often underestimate the duration of
tick attachment because small ticks may not be detected immediately [12,53,54].
A report from California asserting that three patients developed Lyme disease after less than
24 h of tick attachment raises questions about previous transmission studies [
19
]. The aforementioned
study does not address potential issues, such as previous tick bites, and the duration of tick attachment
as noted by critics of the study [
55
57
]. The same report also failed to diagnose Lyme disease using
the Centers for Disease Control and Prevention’s recommended two-tiered algorithm [
58
,
59
], leading
others to question the accuracy of the tick attachment time as related to the development of Lyme
disease [
56
,
57
]. It is possible that there is a difference in the attachment time required for transmission
of B. burgdorferi by nymphs and adult females.
3.4. Borrelia turicatae, B. hermsii (Tick-borne Relapsing Fever)
Tick-borne relapsing fever (TBRF) was first recognized in the US in 1915 [
60
]. This illness
results from infection by Borrelia spp. transmitted by soft ticks (Ornithodoros spp.). Borrelia hermsii
Davis is transmitted to humans by Ornithodoros hermsi Wheeler [
61
,
62
]. Soft ticks attach to hosts
for blood feeding for 10–45 min and spirochetes can be found in salivary glands three days after
feeding on an infectious blood meal [
34
]. Mouse studies have shown transmission of B. hermsii within
30 s of attachment. Transmission of Borrelia turicatae Brumpt has been observed within 15 s after
attachment [
31
]. The same study showed that, for blood meals interrupted after 15 s, the transmission
rate increased when three infected ticks (transmission rate 42–58%) were placed on a single mouse,
compared to when one or two infected ticks (transmission rate 20%) were placed on a single mouse.
This could indicate a greater pathogen dose being introduced into the host due to a greater number of
co-feeding infectious ticks. It has also been indicated that O. turicatae may not transmit B. turicatae at
every blood feeding, although the reason is unclear [
38
]. This may impact assessments of infection
and transmission rates, if the tick is not able to consistently transmit the pathogen, even when the tick
has previously transmitted the pathogen. It is not known whether or not B. turicatae and B. hermsii are
transmitted transovarially.
3.5. Borrelia mayonii (Borreliosis)
Borrelia mayonii Pritt is a recently discovered species within B. burgdorferi senso lato complex
and has been detected in field-collected I. scapularis [
39
,
63
]. From 2012–2014, six patients in the
midwestern region of the US experienced Lyme borreliosis that was attributed to B. mayonii [
63
].
A vector competence study showed that transmission of B. mayonii was more common after infected I.
Environments 2017,4, 37 7 of 14
scapularis were attached to mice for 72–96 h (3/5 mice became infected), compared to 24–48 h (1/6 mice
became infected) of attachment [
39
]. In the same study, six infected ticks were feeding on each naïve
mouse, hence, the amount of the pathogen being inoculated into each mouse by multiple ticks is
expected to vary between replicates. This could have affected differences observed between mice. It is
not known whether or not B. mayonii is transmitted transovarially.
3.6. Borrelia miyamotoi (Borrelia myamotoi Disease, Borreliosis)
Borrelia miyamotoi Fukunaga was isolated from field mice and I. persulcatus in Japan in 1994 [
64
]
and subsequently reported in a US human in 2013 [
65
]. This pathogen is closely related to relapsing
fever spirochetes and this may impact transmission. It has since been detected in US ticks from the
midwest, northeast, south, and west [
66
]. Borrelia miyamotoi is transmitted by I. scapularis and I. pacificus.
Studies have shown that its prevalence in four northeastern states (Connecticut, New Jersey, New York,
Rhode Island) varied from 1.9–2.5% of Ixodes spp. ticks sampled [
67
] and 0.7–1.7% of I. pacificus
ticks tested in California [
68
]. It has been found in ~12% of ticks tested in parts of Indiana [
66
] and
transovarial transmission has been shown in I. scapularis [
52
] and I. ricinus [
69
]. The first cases of
B. miyamotoi-infected humans were reported in Russia in 2011 [
70
,
71
]. A seroprevalence study of
healthy residents of the Northeastern US showed (out of 639 samples), 25 (3.9%) people were exposed
to B. miyamotoi and were antibody-positive and 60 (9.4%) were positive for B. burgdorferi antibodies [
72
].
An attachment study allowed transovarially-infected I. scapularis to blood feed on mice for 24, 48,
72, and 73–96 h [
40
]. The same study showed 10% of mice infected with B. miyamotoi after a 24 h
attachment time, 31% infected at 48 h, 63% infected by 72 h, and 73% of mice were infected by 73–96 h.
3.7. Francisella tularensis (Tularemia)
Francisella tularensis bacteria cause tularemia and Dermacentor andersoni Stiles is the primary
arthropod vector of this pathogen to humans; however, Amblyomma americanum L., D. variabilis [
73
],
and Haemaphysalis leporispalustris Packard are also potential vectors [
34
]. The pathogen can also be
transmitted mechanically by deer flies, horse flies, or mosquitoes, or via aerosol/ingestion when
processing/eating infected animal tissues [
34
,
73
]. Francisella tularensis can be transtadially transmitted
in D. variabilis [
41
] and transtadially and transovarially transmitted (at a low level) in A. americanum [
41
].
However, transovarial transmission is considered uncommon in nature [
73
]. Amblyomma americanum
either inoculated with or fed F. tularensis via capillary tube transmitted infectious saliva into capillary
tubes collected two days post-inoculation [
41
]. However, these ticks were injected with a secretagogue
(hormone-releasing compound) to induce salivation into capillary tubes, hence, this unnatural stimulus
may have impacted the time for pathogen transmission. In the same study, mice injected with
infectious tick saliva became infected; however, transmission directly from ticks to mice was not tested.
In a separate study, four to 11 days after placement on infected Swiss Webster mice, D. variabilis were
assessed for transmission efficiency of three different strains of F. tularensis [
74
]. The transmission
rate for fully blood-fed D. variabilis was 14% for F. tularensis holarctica (type B; strain KY99-3387),
but 0% for two other F. tularensis tularensis strains (MA00-2987; WY96-3418) [
74
]. In the aforementioned
study, ticks were allowed to feed to repletion and duration of tick attachment time required for initial
transmission was not assessed.
3.8. Rickettsia rickettsii (Rocky Mountain Spotted Fever)
RMSF is caused by R. rickettsii transmitted to humans primarily by adult D. variabilis and
D. andersoni. However, R. rickettsii has also been found in field-collected Rhipicephalus sanguineus
Latreille [
75
]. Others also report R. rickettsii-infected, A. americanum,Dermacentor parumapertus
Neumann, and H. leporispalustris [7678].
It takes 15–20 min for a tick to become firmly attached to its host [
78
]. It has been shown that hosts
having R. rickettsii-infected ticks attached for 10–20 h consistently became infected with RMSF [
79
].
Reports show that infectious ticks must be attached for 6–10 h before R. rickettsii is transmitted
Environments 2017,4, 37 8 of 14
via saliva [
80
82
]. Another report shows that guinea pigs exposed to R. rickettsii-infected unfed
Amblyomma aureolatum Pallas nymphs or adults (larvae had previously been infected by feeding on
an infected guinea pig) for
10 h did not become infected [
42
]. The study did not report the degree of
blood feeding (engorgement indices) achieved by the ticks (10 nymphal ticks or 1 adult tick per guinea
pig) but that the countdown began after the first tick became fully attached. The same study showed
all guinea pigs became infected after a 14 h (initially) unfed nymph or adult tick exposure period.
However, partially-fed A. aureolatum adults (male and female ticks fed upon rabbits for 48 h prior to
feeding on guinea pigs) transmitted R. rickettsii to guinea pigs after only ca. 10 min [
42
]. It is during
this blood feeding period [
81
], and/or when ticks are incubated at warm temperatures (37
C) for
24–48 h [
80
], that the bacteria become reactivated from dormancy within tick salivary glands. A study
evaluating transcriptional changes in R. rickettsii contained in A. aureolatum showed five times more
genes (e.g., type IV secretion system and antioxidant enzymes were upregulated) exhibited changes
due to blood feeding versus environmental temperature increases alone, further supporting an increase
in the bacterial load due to blood feeding [83]. This pathogen can be transovarially transmitted [84].
3.9. Heartland Virus
Heartland virus (family Bunyaviridae, genus Phlebovirus) was first reported in humans in 2012 and
is primarily found in Missouri [
85
]. Amblyomma americanum nymphs have been found infected with
Heartland virus; however, no vertebrate reservoir has been confirmed [
86
]. A study infected larval and
nymphal A. americanum by immersing their bodies in a solution of Heartland virus prior to allowing
the ticks to feed on rabbits [
43
]. The same study showed transovarial and transstadial transmission of
Heartland virus, and also the transmission to other ticks through co-feeding. However, no information
was provided about the duration of attachment required for transmission [43].
3.10. Powassan Virus
Powassan virus has been isolated from D. andersoni,Ixodes cookei Packard, Ixodes marxi Banks,
I. scapularis, and Ixodes spinipalpus Hadwin and Nuttall [
34
,
86
,
87
]. POWV-infected I. scapularis nymphs
transmitted the virus to mice in as little as 15 min (63% transmission rate), with maximum transmission
efficiency (83%) achieved after 180 min of attachment [
14
]. It is possible that ticks transmitted POWV
faster than within 15 s since that was the first time point that was checked. In the same study, infected
mice were infested by multiple larval ticks (i.e., 23 mice were infested by 31 POWV-infected ticks)
and ticks (tested after blood feeding) had a range of viral titers (infected larva had a titer range
ca. 0.5–1.5 log
10
plaque-forming units/tick; after molting, infected nymphal ticks had a titer range
ca. 0.25–5.5 log
10
plaque-forming units/tick). One naïve mouse did not become infected after being
fed upon by two infected nymphal ticks [
14
]. This indicates transmission does not always occur and
may be dependent on virus dose inoculated by the potential vector. It is possible for Powassan virus to
be transmitted transovarially [88].
3.11. Neurotoxin (Tick Paralysis)
Tick paralysis is caused by a neurotoxin transmitted in tick saliva during attachment by several
hard and soft tick species [
89
]. Ixovotoxin (related to tick egg production) may be the substance
responsible for tick paralysis [
90
]. The tick must be attached for two to six days for this toxin to take
effect [
91
]. Toxin production coincides with paralytic symptoms and continued tick feeding appears to
accelerate toxin production, accounting for rapid progression of clinical signs [
90
,
92
]. In the US, ticks
that have been implicated in tick paralysis are D. andersoni and D. variabilis. It is also associated with
A. americanum,Amblyomma maculatum Koch, I. pacificus, and I. scapularis.
3.12. Galactose-α-1,3-Galactose (Mammalian Meat Allergy-Alpha-Gal Syndrome)
Alpha-gal syndrome is caused in humans when, during blood feeding, ticks expectorate (in saliva)
the carbohydrate galactose-
α
-1,3-galactose (alpha-gal) and antibodies are produced in the human [
93
].
Environments 2017,4, 37 9 of 14
If humans with alpha-gal antibodies ingest mammalian meat, allergic symptoms may result. In the US,
alpha-gal syndrome has become most common in the southeast [
93
] and meat allergies (e.g., beef,
lamb, pork, venison, cow milk) are associated with A. americanum prevalence [
94
]. It is unknown how
long a tick must be attached in order for the alpha-gal sensitivity to occur. It is thought that meat
allergies would lessen over time if further tick bites were prevented [
93
]; however, more research must
be done to verify this.
4. Discussion
Unlike mosquito-borne viruses that rely solely on the transfer of infectious saliva for propagation
in vertebrate hosts, hard and soft ticks can transmit pathogens (viruses, bacteria, protozoa) via saliva,
regurgitation of gut contents, and also via the cement-like secretion (hard ticks) used to secure itself to
the host [
26
]. Tick-borne diseases are an important health threat that continues to impact public health
worldwide. The impact of tick-borne pathogens may be more extensive than currently understood
due to factors such as nonspecific symptoms experienced during other illnesses, lack of adequate
surveillance systems, and climatic variables impacting tick and animal behaviors [
95
,
96
]. Furthermore,
emerging and re-emerging tick-borne pathogens necessitate the push for further research in this area
to protect public health.
For tick-pathogen systems where published data exists on duration of tick attachment times,
variation was observed between different pathogens and most assessments were conducted on
nonhuman vertebrates, such as rodents. For hard ticks, the duration of attachment required
for transmission of the virus evaluated here was shorter (15–30 min-POWV) than for bacteria
(4–96 h-multiple species evaluated), protozoan (7–18 days-Babesia microti), and neurotoxin (5–7 days).
For soft ticks, we found information on the duration of attachment time (15 s–30 min) required
for transmission of Borrelia turicata and this was a relatively short time period (similar to POWV
transmission by hard ticks) that related to the nature of soft ticks to have brief blood feeding periods,
compared to longer feeding periods required by hard ticks.
Most studies involve placing multiple ticks on multiple rodents, rather than a single tick on
a single rodent, hence, adding further complexity to the comparison of transmission rates and
duration of attachment time required for transmission between studies. Multiple ticks may be
simultaneously delivering different pathogen doses to the host, therefore, in these cases, the host
infection rate cannot be tied to one dose delivered by one tick. Furthermore, some studies assess the
bacteremia or viremia in ticks that fed upon mice, but others determine only the status of infection
in mice that were fed upon and not ticks. Rarely do studies determine the titer of both tick and
host, making it difficult to make a connection between the pathogen dose delivered by the tick
and the infection rate of the host. We expect further variation to exist in vector competence due
to the pathogen dose transmitted by ticks to hosts, biological and/or environmental conditions,
pathogen/vector/host species and population, age of victims, and other unidentified factors. In order
to improve species- and population-specific risk assessments of pathogen transmission to humans
and other animals, more focused experimentally-controlled vector competence research is needed
for tick-borne pathogens. Laboratory experiments are not always an indication of field conditions;
however, laboratory vector competence studies could provide a basis and starting point for field
assessments of risk.
We could not find any published tick attachment time data for the following pathogens: Southern
tick associated rash illness, Borrelia parkeri Davis, Coxiella burnetii,Ehrlichia chaffeensis Anderson,
Ehrlichia ewingii Ewing, Ehrlichia muris Wen, Rickettsia 364D, Rickettsia montanensis Lackman, Rickettsia
parkeri Lackman, and Colorado tick fever virus. Workers in outdoor occupations, such as forestry and
the military, as well as those spending time outdoors participating in recreational activities, should be
aware of the relationship between tick attachment time and the potential for pathogen transmission.
Tick exposure does not always result in pathogen transmission and disease; however, the health threat
exists and individuals should be aware of how to prevent and/or mitigate these risks.
Environments 2017,4, 37 10 of 14
5. Conclusions
The current analysis of published literature reveals knowledge gaps in the duration of tick feeding
time required for pathogen transmission. For tick-pathogen systems where published data exists on
duration of tick attachment times, variation was observed between systems and most evaluations
were conducted on nonhuman vertebrates. We expect further variation for different pathogen doses,
biological and/or environmental conditions, pathogen/vector/host species and population, age of
victims, and other unidentified factors. More research is needed to clarify tick vector competence
for pathogens, duration of tick attachment time required to transmit pathogens, tick species able to
transmit multiple pathogens, etc. to improve risk assessment for this potentially underestimated public
health threat.
Acknowledgments:
This research did not receive any specific grant from funding agencies in the public,
commercial, or not-for-profit sectors. The authors thank two anonymous reviewers for their comments that
improved the manuscript.
Author Contributions:
Ricky Langley conceived and designed the review. Stephanie L. Richards, Ricky Langley,
Charles S. Apperson, and Elizabeth Watson analyzed the data. Stephanie L. Richards wrote the paper.
Stephanie L. Richards, Ricky Langley, Charles S. Apperson, and Elizabeth Watson edited the paper.
Conflicts of Interest: The authors declare no conflict of interest.
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2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
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(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
... Cellular and molecular developmental and physiological interactions occur between the pathogen and the tick vector, including during the blood feeding phase (41,99). Impacted by developmental events within the tick, an important parameter related to these phenomena is the duration of tick blood feeding prior to successful passage of an infectious agent into the bite site and establishment of infection (9,100). These parameters have practical implications for disease prevention. ...
... Variations occur in duration of ixodid tick feeding prior to transmission of a specific tick-borne pathogen as well as for different pathogens (100). B. burgdorferi transmission is well-studied in regard to development within the feeding tick and transmission to a vertebrate host by the North American vector, I. scapularis (100,104,105). ...
... Variations occur in duration of ixodid tick feeding prior to transmission of a specific tick-borne pathogen as well as for different pathogens (100). B. burgdorferi transmission is well-studied in regard to development within the feeding tick and transmission to a vertebrate host by the North American vector, I. scapularis (100,104,105). Nymphs and adults transmit spirochetes, with nymphs transmitting the majority of infections (106,107). ...
Article
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Ticks and tick transmitted infectious agents are increasing global public health threats due to increasing abundance, expanding geographic ranges of vectors and pathogens, and emerging tick-borne infectious agents. Greater understanding of tick, host, and pathogen interactions will contribute to development of novel tick control and disease prevention strategies. Tick-borne pathogens adapt in multiple ways to very different tick and vertebrate host environments and defenses. Ticks effectively pharmacomodulate by its saliva host innate and adaptive immune defenses. In this review, we examine the idea that successful synergy between tick and tick-borne pathogen results in host immune tolerance that facilitates successful tick infection and feeding, creates a favorable site for pathogen introduction, modulates cutaneous and systemic immune defenses to establish infection, and contributes to successful long-term infection. Tick, host, and pathogen elements examined here include interaction of tick innate immunity and microbiome with tick-borne pathogens; tick modulation of host cutaneous defenses prior to pathogen transmission; how tick and pathogen target vertebrate host defenses that lead to different modes of interaction and host infection status (reservoir, incompetent, resistant, clinically ill); tick saliva bioactive molecules as important factors in determining those pathogens for which the tick is a competent vector; and, the need for translational studies to advance this field of study. Gaps in our understanding of these relationships are identified, that if successfully addressed, can advance the development of strategies to successfully disrupt both tick feeding and pathogen transmission.
... Cellular and molecular developmental and physiological interactions occur between the pathogen and the tick vector, including during the blood feeding phase (41,99). Impacted by developmental events within the tick, an important parameter related to these phenomena is the duration of tick blood feeding prior to successful passage of an infectious agent into the bite site and establishment of infection (9,100). These parameters have practical implications for disease prevention. ...
... Variations occur in duration of ixodid tick feeding prior to transmission of a specific tick-borne pathogen as well as for different pathogens (100). B. burgdorferi transmission is well-studied in regard to development within the feeding tick and transmission to a vertebrate host by the North American vector, I. scapularis (100,104,105). ...
... Variations occur in duration of ixodid tick feeding prior to transmission of a specific tick-borne pathogen as well as for different pathogens (100). B. burgdorferi transmission is well-studied in regard to development within the feeding tick and transmission to a vertebrate host by the North American vector, I. scapularis (100,104,105). Nymphs and adults transmit spirochetes, with nymphs transmitting the majority of infections (106,107). ...
... The risk of transmission of a tick-borne bacterial pathogen increases with the duration of attachment of the tick on humans. Indeed, an infected tick generally needs 12-24 h to transmit a bacterium, e.g., Borrelia burgdorferi sl., and few minutes or hours to transmit a virus [18]. A vaccine exists against tick-borne encephalitis, but for other tick-borne diseases transmitted by Ixodes ricinus ticks, the best prevention method relies in preventing tick bites, or at least encouraging tick checks after a risky activity [14,19]. ...
... Similarly, we calculated the overall participation rate in the study and on the banner study for all the racings rounds by calculating the proportion of orienteers who participated at least in one racing round in the study or the banner study. To assess potential biases of recruitment, we compared age and gender profile between participating orienteers and the overall orienteer population of the competition using the following age classes: (7)(8)(9)(10)(11)(12)(13)(14)(15), (15)(16)(17)(18)(19)(20), (20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33)(34)(35), (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50), (50)(51)(52)(53)(54)(55)(56)(57)(58)(59)(60)(61)(62)(63)(64)(65), >65. ...
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Mass-participation events in temperate forests are now well-established features of outdoor activities and represent high-risk activities regarding human exposition to tick bites. In this study we used a citizen science approach to quantify the space–time frequency of tick bites and undetected tick bites among orienteers that participated in a 6-day orienteering competition that took place in July 2018 in the forests of Eastern France, and we looked at the use and efficacy of different preventive behaviors. Our study confirms that orienteers are a high-risk population for tick bites, with 62.4% of orienteers bitten at least once during the competition, and 2.4 to 12.1 orienteers per 100 orienteers were bitten by ticks when walking 1 km. In addition, 16.7% of orienteers bitten by ticks had engorged ticks, meaning that they did not detect and remove their ticks immediately after the run. Further, only 8.5% of orienteers systematically used a repellent, and the use of repellent only partially reduced the probability of being bitten by ticks. These results represent the first attempt to quantify the risk of not immediately detecting a tick bite and provide rare quantitative data on the frequency of tick bites for orienteers according to walking distance and time spent in the forest. The results also provide information on the use of repellent, which will be very helpful for modeling risk assessment. The study also shows that prevention should be increased for orienteers in France.
... De modo geral, qualquer indivíduo, sem imunidade previa frente a Rickettsia parkeri, pode ser susceptível à infecção e, em decorrência, ao padecimento da doença. A picada por um carrapato infectado com R. parkeri destaca-se como a principal via de transmissão, porém, ainda é desconhecido o tempo mínimo de fixação do artrópode para a inoculação do microrganismo no hospedeiro susceptível (RICHARDS et al., 2017); acredita-se que esse tempo é inferior a oito horas (WHITMAN et al., 2007). ...
... De modo geral, qualquer indivíduo, sem imunidade previa frente a Rickettsia parkeri, pode ser susceptível à infecção e, em decorrência, ao padecimento da doença. A picada por um carrapato infectado com R. parkeri destaca-se como a principal via de transmissão, porém, ainda é desconhecido o tempo mínimo de fixação do artrópode para a inoculação do microrganismo no hospedeiro susceptível (RICHARDS et al., 2017); acredita-se que esse tempo é inferior a oito horas (WHITMAN et al., 2007). ...
... De modo geral, qualquer indivíduo, sem imunidade previa frente a Rickettsia parkeri, pode ser susceptível à infecção e, em decorrência, ao padecimento da doença. A picada por um carrapato infectado com R. parkeri destaca-se como a principal via de transmissão, porém, ainda é desconhecido o tempo mínimo de fixação do artrópode para a inoculação do microrganismo no hospedeiro susceptível (RICHARDS et al., 2017); acredita-se que esse tempo é inferior a oito horas (WHITMAN et al., 2007). ...
... Ticks are the primary vectors for pathogens of domesticated and wild animals and the secondary vectors for pathogens of humans [30]. Tick-bites are considered an occupational health issue for forestry personnel and others working (e.g., agricultural industry, military) and/or participating in recreational activities (e.g., hunting, hiking) in forested areas [37]. Since the beginning of this century, tick-borne viral diseases increasingly have been reported in many parts of the world, with examples including Alkhurma haemorrhagic fever [2], African swine fever [36], Crimean-Congo haemorrhagic fever [23], severe fever with thrombocytopenia syndrome (SFTS) virus [38], Heartland virus infection [30], Powassan virus infection [13], Kyasasur forest disease [1], Yezo virus infection [21], Oz virus [7,42] and so on. ...
Article
Kabuto Mountain virus (KAMV), the new member of the genus Uukuvirus, was isolated from the tick Haemaphysalis flava in 2018 in Japan. To date, there is no information on KAMV infection in human and animals. Therefore, serological surveillance of the infection among humans and wild mammals was conducted by virus-neutralization (VN) test and indirect immunofluorescence assay (IFA). Sera of 24 humans, 59 monkeys, 171 wild boars, 233 Sika deer, 7 bears, and 27 nutria in Yamaguchi Prefecture were analyzed by VN test. The positive ratio of humans, monkeys, wild boars, and Sika deer were 20.8%, 3.4%, 33.9% and 4.7%, respectively. No positive samples were detected in bears and nutria. The correlation coefficients between VN test and IFA in human, monkey, wild boar, and Sika deer sera were 0.5745, 0.7198, 0.9967 and 0.9525, respectively. In addition, KAMV was detected in one pool of Haemaphysalis formosensis ticks in Wakayama Prefecture. These results indicated that KAMV or KAMV-like virus is circulating among many wildlife and ticks, and that this virus incidentally infects humans.
... Pour avoir une idée de l'ordre de grandeur des temps de transmission d'autre agents infectieux transmis par les tiques, voir Richards et al. (2017), bien que ne concernant que l'Amérique du Nord. Pour les virus, la transmission peut se produire en moins d'une heure, pour les bactéries plusieurs heures sont généralement nécessaires (quelques minutes chez les tiques molles), et pour les parasite eucaryotes unicellulaires plus d'un jour. ...
Technical Report
Dans le cadre du plan national de prévention et de lutte contre la maladie de Lyme et les maladies transmissibles par les tiques (« Plan Lyme »)1, lancé en 2016, un projet de recherche bibliographique sur l’écologie, la surveillance et la lutte contre les tiques présentes en France métropolitaine et responsables de maladies infectieuses humaines zoonotiques dont la borréliose de Lyme, a été commandité à l’ANSES par la Direction Générale de la Santé. Ce projet a été confié à l’École nationale vétérinaire d’Alfort dans le cadre d’une Convention de Recherche et Développement (CRD). Pour le mener à bien, un post-doctorant a été recruté sur un contrat d’un an et un mois (du 14 octobre 2019 au 13 novembre 2020) au sein de l’UMR BIPAR (EnvA – ANSES – INRAE). Full text available at: https://hal.archives-ouvertes.fr/anses-03263410/
... Self-grooming in cats (i.e., ;8% of their nonsleeping time, ;4% of their entire life) (351) serves as a preventative mechanism against ectoparasites (Fig. 1), especially ticks (351,352). As, in most cases, ticks must be attached for a while before transmitting pathogens, cats that promptly remove ticks by self-grooming are rarely infected by TBPs (115,353). Hepatozoonosis is an exception, as it is one of the most frequent feline VBDs in certain areas (354), acquired by tick ingestion facilitated by self-grooming (355,356). ...
Article
Cats and dogs are treated as family members by most pet owners. Therefore, a high quality of veterinary care and preventive medicine is imperative for animal health and welfare and for the protection of humans from zoonotic pathogens. There is a general perception of cats being treated as “small dogs,” especially in the field of clinical parasitology. As a result, several important differences between the two animal species are not taken into proper consideration and are often overlooked. Dogs and cats are profoundly different under evolutionary, biological, ethological, behavioral, and immunological standpoints. These differences impact clinical features, diagnosis, and control of canine and feline parasites and transmission risk for humans. This review outlines the most common parasitoses and vector-borne diseases of dogs and cats, with a focus on major convergences and divergences, and discusses parasites that have (i) evolved based on different preys for dogs and cats, (ii) adapted due to different immunological or behavioral animal profiles, and (iii) developed more similarities than differences in canine and feline infections and associated diseases. Differences, similarities, and peculiarities of canine and feline parasitology are herein reviewed in three macrosections: (i) carnivorism, vegetarianism, anatomy, genetics, and parasites, (ii) evolutionary adaptation of nematodes, including veterinary reconsideration and zoonotic importance, and (iii) behavior and immune system driving ectoparasites and transmitted diseases. Emphasis is given to provide further steps toward a more accurate evaluation of canine and feline parasitology in a changing world in terms of public health relevance and One Health approach.
... In contrast, the tick digests its blood meal inside the midgut cells; therefore, the midgut lumen provides a barrier to viruses that requires proteolytic enzymes to infect midgut cells (Nuttall, 2009;Sojka et al., 2013). On the other hand, tick-borne viruses are also protected from numerous proteases secreted into the midgut lumen since they will first encounter an acidic environment within endosomes of the midgut cells (Nuttall, 2009;Richards et al., 2017;Sonenshine and Roe, 2014). ...
Article
Ticks, being obligate hematophagous arthropods, are exposed to various blood-borne pathogens, including arboviruses. Consequently, their feeding behavior can readily transmit economically important viral pathogens to humans and animals. With this tightly knit vector and pathogen interaction, the replication and transmission of tick-borne viruses (TBVs) must be highly regulated by their respective tick vectors to avoid any adverse effect on the ticks’ biological development and viability. Knowledge about the tick–virus interface, although gaining relevant advances in recent years, is advancing at a slower pace than the scientific developments related to mosquito–virus interactions. The unique and complicated feeding behavior of ticks, compared to that of other blood-feeding arthropods, also limits the studies that would further elaborate the antiviral immunity of ticks against TBVs. Hence, knowledge of molecular and cellular immune mechanisms at the tick–virus interface, will further elucidate the successful viral replication of TBVs in ticks and their effective transmission to human and animal hosts.
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Rickettsia rickettsii – the etiologic agent of Rocky Mountain spotted fever (RMSF) – is widely spread across the Americas. In the US, Dermacentor spp. ticks are identified as primary vectors of R. rickettsii and Rhipicephalus sanguineus s.l. has been implicated in transmission of this pathogen in several locations in the Southwest. Conversely, ticks of the genus Amblyomma are recognized vectors of RMSF in Central and South America, but not in the US. A. americanum is one of the most aggressive human-biting ticks in the US, whose geographical range overlaps with that of reported RMSF cases. Despite sporadic findings of R. rickettsii DNA in field-collected A. americanum and circumstantial association of this species with human RMSF cases, its vector competence for R. rickettsii has not been appropriately studied. Therefore, we assessed the ability of A. americanum to acquire and transmit two geographically distant isolates of R. rickettsii. The Di-6 isolate of R. rickettsii used in this study originated in Virginia and the AZ-3 isolate originated in Arizona. Under laboratory conditions, A. americanum demonstrated vector competence for both isolates, although the efficiency of acquisition and transovarial transmission was higher for Di-6 than for AZ-3 isolate. Uninfected larvae acquired the pathogen from systemically infected guinea pigs, as well as while feeding side by side with Rickettsia-infected ticks on non-rickettsiemic hosts. Once acquired, R. rickettsii was successfully maintained through the tick molting process and transmitted to susceptible animals during subsequent feedings. Guinea pigs and dogs infested with infected A. americanum developed fever, scrotal edema and dermatitis or macular rash. R. rickettsii DNA was identified in animal blood, skin, and internal organs. The prevalence of infection within tick cohorts gradually increased due to side-by-side feeding of infected and uninfected individuals from 33–49% in freshly molted nymphs to 71–98% in engorged females. Moreover, R. rickettsii was transmitted transovarially by approximately 28% and 14% of females infected with Di-6 and AZ-3 isolates respectively. Hence, A. americanum is capable of acquiring, maintaining and transmitting R. rickettsii isolates originating from two different geographical regions of the US, at least under laboratory conditions. Its role in ecology and epidemiology of RMSF in the US deserves further investigation.
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Borrelia miyamotoi sensu lato relapsing fever group spirochetes are emerging as causative agents of human illness (Borrelia miyamotoi disease) in the United States. Host-seeking Ixodes scapularis ticks are naturally infected with these spirochetes in the eastern United States and experimentally capable of transmitting B. miyamotoi. However, the duration of time required from tick attachment to spirochete transmission has yet to be determined. We therefore conducted a study to assess spirochete transmission by single transovarially infected I. scapularis nymphs to outbred white mice at three time points post-attachment (24, 48, and 72 hours) and for a complete feed ( > 72–96 hours). Based on detection of B. miyamotoi DNA from the blood of mice fed on by an infected nymph, the probability of spirochete transmission increased from 10% by 24 hours of attachment (evidence of infection in 3/30 mice) to 31% by 48 hours (11/35 mice), 63% by 72 hours (22/35 mice), and 73% for a complete feed (22/30 mice). We conclude that (i) single I. scapularis nymphs effectively transmit B. miyamotoi relapsing fever group spirochetes while feeding, (ii) transmission can occur within the first 24 hours of nymphal attachment, and (iii) the probability of transmission increases with the duration of nymphal attachment.
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