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A STING from a Tick: Epidemiology, Ecology and Clinical Aspects of Lyme Borreliosis
Linköping University, Department of Clinical and Experimental Medicine, Division of Microbiology and Molecular Medicine. Linköping University, Faculty of Health Sciences.
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Lyme borreliosis (LB) is the most common tick-borne disease in the Northern Hemisphere and the number of LB cases is increasing. The infection is caused by spirochetes belonging to the Borrelia burgdorferi sensu lato complex, and is, in Europe, transmitted to humans by Ixodes ricinus ticks.

To gain a deeper knowledge of the interactions between ticks, humans and Borrelia bacteria, we investigated temporal differences in exposure to tick bites in different parts of Sweden and the Åland Islands, Finland during the years 2008 and 2009. We also investigated the site of tick attachment on the human body and the time it takes for a person to detected and remove such ticks. Furthermore, the distribution of Borrelia species and the number of Borrelia cells in the ticks were investigated. Sera taken from the tick-bitten persons at study inclusion were analyzed for the presence of Borrelia antibodies. Three months later, the clinical outcome and the serological response of the tick-bitten persons were investigated. A total of 2154 I. ricinus ticks and 1546 participants were included in the studies.

Participants were exposed to tick bites between April and November, but temporal and spatial differences in exposure to ticks was found. The majority of the tick bites were caused by nymphs (70%) and most tick bites took place on the legs (50%). The site of tick attachment on the body as well as the age and gender of the participant influenced how soon a tick was detected. The majority of participants removed “their” ticks later than 24 hours of attachment. Of all ticks, 26% was Borrelia-infected, but the prevalence varied between the life stages of the tick and between the studied areas. Six species of the B. burgdorferi sensu lato complex and one Borrelia species that may cause tick-borne relapsing fever were detected. Adult ticks that had fed more than 36 hours contained a lower number of Borrelia cells than adult ticks that had fed less than 36 hours. The seroprevalence among the participants varied between genders as well as between the studied areas. Of all participants, 2% was diagnosed with LB and 2.5% seroconverted without an LB diagnose. A correlation between seroconversion and duration time of tick attachment was found, but the number of Borrelia cells in the tick, did not explain the risk of infection for the bitten person.

A deeper knowledge and a better understanding of the interactions between ticks, humans and Borrelia bacteria may contribute reducing the risk for tick bites and the risk of developing LB after a tick bite.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press, 2014. , 130 p.
Series
Linköping University Medical Dissertations, ISSN 0345-0082 ; 1385
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:liu:diva-105476DOI: 10.3384/diss.diva-105476ISBN: 978-91-7519-460-8 (print)OAI: oai:DiVA.org:liu-105476DiVA: diva2:707600
Public defence
2014-04-24, Berzeliussalen, Campus US, Linköpings universitet, Linköping, 09:00 (English)
Opponent
Supervisors
Available from: 2014-03-25 Created: 2014-03-25 Last updated: 2014-04-04Bibliographically approved
List of papers
1. Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding
Open this publication in new window or tab >>Ixodes ricinus ticks removed from humans in Northern Europe: seasonal pattern of infestation, attachment sites and duration of feeding
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2013 (English)In: Parasites & Vectors, ISSN 1756-3305, E-ISSN 1756-3305, Vol. 6, no 362Article in journal (Refereed) Published
Abstract [en]

BACKGROUND:

The common tick Ixodes ricinus is the main vector in Europe of the tick-borne encephalitis virus and of several species of the Borrelia burgdorferi sensu lato complex, which are the etiological agents of Lyme borreliosis. The risk to contract bites of I. ricinus is dependent on many factors including the behaviour of both ticks and people. The tick's site of attachment on the human body and the duration of tick attachment may be of clinical importance. Data on I. ricinus ticks, which were found attached to the skin of people, were analysed regarding potentially stage-specific differences in location of attachment sites, duration of tick attachment (= feeding duration), seasonal and geographical distribution of tick infestation in relation to age and gender of the tick-infested hosts.

METHODS:

During 2008-2009, 1770 tick-bitten persons from Sweden and the Åland Islands removed 2110 I. ricinus ticks. Participants provided information about the date of tick detection and location on their body of each attached tick. Ticks were identified to species and developmental stage. The feeding duration of each nymph and adult female tick was microscopically estimated based on the scutal and the coxal index.

RESULTS:

In 2008, participants were tick-bitten from mid-May to mid-October and in 2009 from early April to early November. The infestation pattern of the nymphs was bimodal whereas that of the adult female ticks was unimodal with a peak in late summer. Tick attachment site on the human body was associated with stage of the tick and gender of the human host. Site of attachment seemed to influence the duration of tick feeding. Overall, 63% of nymphs and adult female ticks were detected and removed more than 24 hours after attachment. Older persons, compared to younger ones, and men, compared to women, removed "their" ticks after a longer period of tick attachment.

CONCLUSIONS:

The infestation behaviour of the different tick stages concerning where on the host's body the ticks generally will attach and when such ticks generally will be detected and removed in relation to host age and gender, should be of value for the development of prophylactic methods against tick infestation and to provide relevant advice to people on how to avoid or reduce the risk of tick infestation.

Place, publisher, year, edition, pages
BioMed Central, 2013
Keyword
Ixodes ricinus; Tick infestation; Tick bite; Attachment site; Feeding behaviour; Feeding duration; Host-seeking behaviour; Seasonal activity; Sweden; Åland
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-103499 (URN)10.1186/1756-3305-6-362 (DOI)000330064200001 ()24360096 (PubMedID)
Available from: 2014-01-20 Created: 2014-01-20 Last updated: 2017-12-06Bibliographically approved
2. Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden
Open this publication in new window or tab >>Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden
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2010 (English)In: JOURNAL OF CLINICAL MICROBIOLOGY, ISSN 0095-1137, Vol. 48, no 11, 4169-4176 p.Article in journal (Refereed) Published
Abstract [en]

Members of the genus Borrelia are among the most common infectious agents causing tick-borne disease in humans worldwide. Here, we developed a Light Upon eXtension (LUX) real-time PCR assay that can detect and quantify Borrelia species in ticks that have fed on humans, and we applied the assay to 399 such ticks. Borrelia PCR-positive ticks were identified to species level by sequencing the products of conventional PCR performed using Borrelia group-specific primers. There was a 19% prevalence of Borrelia spp. in the detached ticks, and the number of spirochetes per Borrelia PCR-positive tick ranged from 2.0 x 10(2) to 4.9 x 10(5), with a median of 7.8 x 10(3) spirochetes. Adult ticks had a significantly larger number of spirochetes, with a median of 8.4 x 10(4) compared to the median of nymphs of 4.4 x 10(4). Adult ticks also exhibited a higher prevalence of Borrelia (33%) than nymphs (14%). Among the identified species, Borrelia afzelii was found to predominate (61%) and was followed by B. garinii (23%), B. valaisiana (13%), B. burgdorferi sensu stricto (1%), B. lusitaniae (1%), and B. miyamotoi-like (1%). Also, 3% of the ticks were coinfected with multiple strains of B. afzelii. Notably, this is the first report of B. lusitaniae being detected in ticks in Sweden. Our LUX real-time PCR assay proved to be more sensitive than a corresponding TaqMan assay. In conclusion, the novel LUX real-time PCR method is a rapid and sensitive tool for detection and quantification of Borrelia spp. in ticks.

Place, publisher, year, edition, pages
American Society for Microbiology, 2010
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-62152 (URN)10.1128/JCM.01061-10 (DOI)000283588500049 ()
Note
Original Publication: Peter Wilhelmsson, Linda Fryland, Stefan Börjesson, Johan Nordgren, Sven Bergström, Jan Ernerudh, Pia Forsberg and Per-Eric Lindgren, Prevalence and Diversity of Borrelia Species in Ticks That Have Bitten Humans in Sweden, 2010, JOURNAL OF CLINICAL MICROBIOLOGY, (48), 11, 4169-4176. http://dx.doi.org/10.1128/JCM.01061-10 Copyright: American Society for Microbiology http://www.asm.org/ Available from: 2010-11-19 Created: 2010-11-19 Last updated: 2014-03-25
3. Prevalence, Diversity, and Load of Borrelia species in Ticks That Have Fed on Humans in Regions of Sweden and Åland Islands, Finland with Different Lyme Borreliosis Incidences
Open this publication in new window or tab >>Prevalence, Diversity, and Load of Borrelia species in Ticks That Have Fed on Humans in Regions of Sweden and Åland Islands, Finland with Different Lyme Borreliosis Incidences
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2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 11, e81433- p.Article in journal (Refereed) Published
Abstract [en]

The incidence of Lyme borreliosis (LB) in a region may reflect the prevalence of Borrelia in the tick population. Our aim was to investigate if regions with different LB incidences can be distinguished by studying the prevalence and diversity of Borrelia species in their respective tick populations. The Borrelia load in a feeding tick increases with the duration of feeding, which may facilitate a transmission of Borrelia Spirochetes from tick to host. Therefore, we also wanted to investigate how the Borrelia load in ticks that have fed on humans varies with the duration of tick feeding. During 2008 and 2009, ticks that had bitten humans were collected from four regions of Sweden and Finland, regions with expected differences in LB incidence. The duration of tick feeding was estimated and Borrelia were detected and quantified by a quantitative PCR assay followed by species determination. Out of the 2,154 Ixodes ricinus ticks analyzed, 26% were infected with Borrelia and seven species were identified. B. spielmanii was detected for the first time in the regions. The tick populations collected from the four regions exhibited only minor differences in both prevalence and diversity of Borrelia species, indicating that these variables alone cannot explain the regions different LB incidences. The number of Borrelia cells in the infected ticks ranged from fewer than ten to more than a million. We also found a lower number of Borrelia cells in adult female ticks that had fed for more than 36 hours, compared to the number of Borrelia cells found in adult female ticks that had fed for less than 36 hours.

Place, publisher, year, edition, pages
Public Library of Science, 2013
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-102779 (URN)10.1371/journal.pone.0081433 (DOI)000327539800130 ()
Note

Funding Agencies|Medical Research Council of South-East Sweden|FORSS-8967FORSS-12573FORSS-29021FORSS-86911|Swedish Research Council (Medicine)|2011-345|County Council of Ostergotland||Wilhelm and Else Stockmanns Foundation||Angstromlands Kuturstiftelse||EU Interreg IV A|167226|

Available from: 2014-01-07 Created: 2013-12-26 Last updated: 2017-12-06
4. A prospective study on the incidence of Borrelia infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)
Open this publication in new window or tab >>A prospective study on the incidence of Borrelia infection after a tick bite in Sweden and on the Åland Islands, Finland (2008-2009)
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2016 (English)In: Ticks and Tick-borne Diseases, ISSN 1877-959X, E-ISSN 1877-9603, Vol. 7, no 1, 71-79 p.Article in journal (Refereed) Published
Abstract [en]

Lyme borreliosis (LB) is a common and increasing tick-borne disease in Europe. The risk of acquiring a Borrelia infection after a tick bite is not fully known. Therefore, we investigated the incidence of Borrelia infection after a tick bite and if the Borrelia load and/or the duration of tick-feeding influenced the risk of infection. During 2008-2009, ticks and blood samples were collected from 1546 tick-bitten persons from Sweden and the Åland Islands, Finland. Follow-up blood samples were taken three months after the tick bite. The duration of tick feeding was microscopically estimated and Borrelia was detected and quantified in ticks by real-time PCR. Anti-Borrelia antibodies were detected in sera using ELISA assays and immunoblot.

Even though 28 % of the participants were bitten by a Borrelia-positive tick, only 7.5% (32/428) of them developed a Borrelia infection, half of them LB. All who seroconverted removed “their” ticks significantly later than those who did not. The Borrelia load in the ticks did not explain the risk of seroconversion. Regional as well as gender differences in the Borrelia seroprevalence were found. The risk of developing a Borrelia infection after a bite by a Borrelia-infected tick is small but increases with the duration of tick feeding.

Place, publisher, year, edition, pages
Elsevier, 2016
Keyword
Borrelia burgdorferi sensu lato; tick bite; incidence of infection; Lyme borreliosis; asymptomatic infection; bacterial load; tick-feeding.
National Category
Infectious Medicine
Identifiers
urn:nbn:se:liu:diva-105475 (URN)10.1016/j.ttbdis.2015.08.009 (DOI)000366953400012 ()
Note

Funding agencies: Swedish Research Council Branch of Medicine [K2008-58X-14631-06-3]; Medical Research Council of South-East Sweden [FORSS-8967, FORSS-12573, FORSS-29021, FORSS-86911]; EU Interreg IV A project ScandTick [167226]; County Council of Ostergotland [LIO-56191];

Available from: 2014-03-25 Created: 2014-03-25 Last updated: 2017-05-03Bibliographically approved

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