Rospotrebnadzor on the spread of infections transmitted with a tick bite in

FAQ: Tick-Borne Diseases

In this Article

In this Article

In this Article

Although Lyme disease is the most prevalent tick-borne infection in the U.S., experts are seeing more serious tick-borne illnesses — some of them fatal if not treated right away.

In 2017, state and local health departments reported a record number of cases of tick-borne disease to the CDC.

Already this summer, health officials in New Jersey are investigating two confirmed cases of Powassan virus — a rare but potentially serious disease spread by the blacklegged or deer tick. Both cases were in Sussex County, in the northwest corner of the state.

A recent CDC report showed that vector-borne diseases — those transmitted by ticks, mosquitoes, and fleas — tripled to roughly 650,000 cases between 2004 and 2016. The vast majority — or 75% — were caused by ticks. The report says seven new tick-caused illnesses were discovered between 2004 and 2016.

It’s difficult to predict from year to year how many cases of tick-borne diseases will be reported in the U.S. The tiny bugs are now in 50 states, and as a result, more people are at risk every spring, summer, and fall.

Here’s what you need to know about tick-borne illnesses.

Q. Are cases of tick-borne illnesses on the rise?

A. From 2004 to 2016, tick-borne diseases, including Rocky Mountain spotted fever, have risen dramatically. In just one year, from 2016 to 2017, cases rose 23%, CDC figures show.

  • Lyme disease: 42,743, up from 19,804 in 2004 (Experts believe the annual number is around 300,000, based on surveillance.)
  • Anaplasmosis/ehrlichiosis: 7,718, up from 875 in 2004
  • Rocky Mountain spotted fever: 6,248, up from 1,713 in 2004
  • Babesiosis: 2,368, up from 1,128 in 2011, when tracking started for the disease
  • Tularemia: 239, up from 134 in 2004
  • Powassan virus: 33, up from 1 in 2004

Q. Where are ticks found?

A. The blacklegged tick — responsible for Lyme disease, the Powassan virus, babesiosis, and anaplasmosis — is found in every state across the eastern U.S. and into Texas, Oklahoma, Kansas, Nebraska, and the Dakotas. The geographic range of other ticks, including the Lone Star, American dog, brown dog, and Rocky Mountain wood tick, has also expanded throughout North America. They cause Rocky Mountain spotted fever, anaplasmosis, ehrlichiosis, and other infections.

Q. How are tick-borne diseases treated?

A. A simple antibiotic, doxycycline, can be used to snuff out most of the diseases — if they are recognized and treated early.

Q. How long does a tick have to stick to you to transmit infections?

A. For Rocky Mountain spotted fever, it takes 2 to 96 hours; for Lyme disease, it depends on the tick. One transmits the infection between 4 and 72 hours; the other from 48-96 hours. For anaplasmosis and ehrlichiosis, a tick needs to be attached for 24 to 50 hours. It is unknown how long a tick needs to be attached to transmit Powassan or Heartland virus.

Q. What is the East Asian or longhorned tick?

A. This tick, discovered on a New Jersey sheep farm in late 2017, is known to transmit severe fever with thrombocytopenia syndrome. This potentially fatal disease causes low platelet and low white blood cell counts. It’s now found in Arkansas, Connecticut, Kentucky, Maryland, North Carolina, New Jersey, New York, Pennsylvania, Tennessee, Virginia, and West Virginia.

Q. What is Rocky Mountain spotted fever, and how is it transmitted?

A. You can get this disease from the American dog tick, the brown dog tick, and the Rocky Mountain wood tick. Five states — North Carolina, Oklahoma, Arkansas, Tennessee, and Missouri — account for more than 60% of the cases. According to the CDC, about 4,000 to 6,000 cases of tick-borne spotted fevers, including Rocky Mountain spotted fever, are reported each year in this region.

But Native American reservations in southeast Arizona have seen epidemic levels of the disease — a result of human contact with stray dogs that carry the ticks.

Between 2003 and 2016, public health officials reported more than 360 cases of Rocky Mountain spotted fever in the region, including 21 deaths.

Q. What are symptoms of Rocky Mountain spotted fever?

A. They aren’t much different from the flu — fever, headache, muscle aches. But within 2-5 days, a rash will begin on your arms and legs and spread to your chest and stomach. At that point, the disease may be doing serious damage to your organs.

Q. How is Rocky Mountain spotted fever treated?

A. Doxycycline is the most effective antibiotic to prevent severe illness and death from Rocky Mountain spotted fever if a patient gets it in the first 5 days of illness. The average time someone dies after showing symptoms is 8 days.

Q: Which other tick-borne diseases are fatal?

A. The death rate from Rocky Mountain spotted fever and anaplasmosis is less than 1%, and it’s about 1% for ehrlichiosis, according to the CDC.

A handful of deaths have been reported from Bourbon, Heartland, and Powassan viruses.

Q. What is the Bourbon virus?

A. The Bourbon virus is likely spread through the bite of a lone star tick or an insect, the CDC says. A handful of cases of the virus have been reported in the Midwest and South, including some that have resulted in death. Symptoms of the virus can include rash, fever, nausea, body aches, tiredness, headache, and vomiting. There is no cure for an infection. Treatment may include IV fluids and pain medications.

Q. What is the Heartland virus?

A. The Heartland virus is caused by the lone star tick. As of September 2018, more than 40 cases have been reported in the Midwest and South, a few of which resulted in death. Symptoms may include fever, headaches, fatigue, muscle aches, and diarrhea. There are no vaccines to prevent this virus or medications to treat it.

Q. What are seed ticks?

A. The phrase “seed ticks” refers to tick larvae. The larvae look like poppy seeds on your skin. Even at this young stage, they can still bite. The bites are commonly painless. The ticks can crawl up your body under clothing and bite you in places that are hard to see.

Q. What is Powassan virus?

A. Unlike some other tick-borne infections, Powassan is a virus. That means antibiotics don’t work to treat it. No antiviral drugs seem to work against it, and there is a high risk of long-term disability and death.

Powassan is rare — only 100 cases reported in the last decade — but its numbers could rise as more people come into contact with ticks. The CDC reported 33 cases in 2017.

Q. Where are the most cases of Powassan reported?

A. Cases are concentrated in the northeast U.S. and in the Great Lakes region.

Q. What are the symptoms of Powassan, and are they different from other tick-borne infections?

A. Powassan strikes with fever, chills, muscle aches, and headache, and as the virus progresses, it can lead to seizures and brain and spinal cord inflammation — conditions that you should go to the hospital for. Unlike other tick-borne diseases, the symptoms of Powassan do not include a rash.

Q. How do you treat the disease?

A. Mainly with supportive care — painkillers for headache, and hospitalization for people with severe illness. It may include breathing support, intravenous fluids and medications to reduce swelling in the brain. Death is rare and happens in about 10% of the cases that have swelling in the brain, or encephalitis. Other patients end up with long-term memory problems, headaches, and muscle wasting.

Q. Can you get a meat allergy from a tick bite?

A. Scientists aren’t yet sure, but there is data linking something called alpha-gal allergy with tick bites. Alpha-gal is a sugar molecule found in most mammals and some type of ticks. People have allergic reactions after they eat meat from mammals that have it or are exposed to products made from mammals. They may include medications, cosmetics, vaccines, gelatin, and milk products.

Most cases have been reported in the Southeast and Midwest. The Lone Star tick is suspected in cases involving red meat.

Symptoms can be severe and life-threatening. They include rash, hives, difficult breathing, a drop in blood pressure, dizziness or fainting, nausea or vomiting, and severe stomach pain. They usually appear about 3 to 6 hours after eating meat or being exposed to products that have it.

The allergic reaction generally happens within 6 months after the tick bite, usually in someone who had no previous allergies. It’s more common in older adults.

Q. How can I prevent tick bites?

A. Prevention is the only way to avoid infection:

  • Limit your exposure to tall grass; walk in the center of trails. Ticks generally latch onto your foot or leg and crawl up your body, often to your head or ears. They don’t jump or fly.
  • Remove leaf litter, and clear tall grass and brush around your home and the edge of your yard.
  • Use a 3-foot-wide barrier of wood chips or gravel between your yard and wooded areas to keep ticks from coming into your yard.
  • Mow your lawn frequently.
  • Keep decks, playground equipment, and patios away from trees and the edge of your yard.
  • Wear insect repellent with 20% or more DEET, picaridin, or IR3535 on skin that is exposed.
  • Treat clothing with the chemical permethrin.
  • If you’ve been outside where ticks may live, do a full-body check once you get in, or examine your skin in the shower. Shower as soon as possible after spending time outdoors.
  • If you see a tick, remove it with tweezers as close to the skin as possible, pulling it straight out. Dispose of it by flushing it down the toilet or throwing it back outside. Don’t crush it between your fingers. If you suspect it’s an Asian longhorned tick, save it in rubbing alcohol in a jar or a zip-close bag, then contact your local health department.
  • Dogs pick up ticks and bring them inside. Check your pet’s skin for ticks, and use tick collars, sprays, shampoos, and medications to prevent ticks.
  • Tumble dry clothes in a dryer on high heat for 10 minutes to kill ticks on dry clothing after you come indoors.

Richard, S. Environments, 2017.

Entomology Today, Jan. 18, 2016.

University of Rhode Island TickEncounter Resource Center.

State of New Jersey Department of Agriculture: “Exotic Tick Species Found in Middlesex County.”

CDC: “Severe Fever with Thrombocytopenia Syndrome Virus, South Korea, 2013.”

Clinical Infectious Diseases, June 1, 2015.

Denise Bonilla, USDA/APHIS, United States Department of Agriculture.

News release, Sussex County, NJ.

Minnesota Department of Health: “Powassan Virus Disease.”

American College of Allergy, Asthma & Immunology: “Meat Allergy.”

HHS Working Group on Lyme and Other Tickborne Diseases webinar: “Emerging Issues in Tickborne Diseases.”

www.webmd.com

Transmission

The Lyme disease bacterium, Borrelia burgdorferi, is spread through the bite of infected ticks. The blacklegged tick (or deer tick, Ixodes scapularis) spreads the disease in the northeastern, mid-Atlantic, and north-central United States. The western blacklegged tick (Ixodes pacificus) spreads the disease on the Pacific Coast.

Ticks can attach to any part of the human body but are often found in hard-to-see areas such as the groin, armpits, and scalp. In most cases, the tick must be attached for 36 to 48 hours or more before the Lyme disease bacterium can be transmitted.

Most humans are infected through the bites of immature ticks called nymphs. Nymphs are tiny (less than 2 mm) and difficult to see; they feed during the spring and summer months. Adult ticks can also transmit Lyme disease bacteria, but they are much larger and are more likely to be discovered and removed before they have had time to transmit the bacteria. Adult Ixodes ticks are most active during the cooler months of the year.

  • There is no ev >External .
  • Although dogs and cats can get Lyme disease, there is no evidence that they spread the disease directly to their owners. However, pets can bring infected ticks into your home or yard. Consider protecting your pet, and possibly yourself, through the use of tick control products for animals.
  • You will not get Lyme disease from eating venison or squirrel meat, but in keeping with general food safety principles, always cook meat thoroughly. Note that hunting and dressing deer or squirrels may bring you into close contact with infected ticks.
  • There is no credible evidence that Lyme disease can be transmitted through air, food, water, or from the bites of mosquitoes, flies, fleas, or lice.
  • Ticks not known to transmit Lyme disease include Lone star ticks (Amblyomma americanum), the American dog tick (Dermacentor variabilis), the Rocky Mountain wood tick (Dermacentor andersoni), and the brown dog tick (Rhipicephalus sanguineus).

Ticks can’t fly or jump. Instead, they wait for a host, resting on the tips of grasses and shrubs in a position known as “questing”. While questing, ticks hold onto leaves and grass by their lower legs. They hold their upper pair of legs outstretched, waiting to climb onto a passing host. When a host brushes the spot where a tick is waiting, it quickly climbs aboard. It then finds a suitable place to bite its host.

The tick feeding process makes ticks very good at transmitting infection:

  • Depending on the tick species and its stage of life, preparing to feed can take from 10 minutes to 2 hours. When the tick finds a feeding spot, it grasps the skin and cuts into the surface. The tick then inserts its feeding tube. Many species also secrete a cement-like substance that keeps them firmly attached during the meal. The feeding tube can have barbs, which help keep the tick in place.
  • Ticks also can secrete small amounts of saliva with anesthetic properties so that the animal or person can’t feel that the tick has attached itself. If the tick is in a sheltered spot, it can go unnoticed.
  • A blacklegged tick will attach to its host and suck the blood slowly for several days. If the host animal has certain bloodborne infections, such as the bacteria that cause Lyme disease, the tick may ingest the pathogen and become infected. If the tick later feeds on a human, that human can become infected.
  • After feeding, the blacklegged tick drops off and prepares for the next life stage. At its next feeding, it can then transmit the infection to the new host. Once infected, a tick can transmit infection throughout its life.
  • If you remove a tick quickly (within 24 hours), you can greatly reduce your chances of getting Lyme disease. It takes some time for the Lyme disease-causing bacteria to move from the tick to the host. The longer the tick is attached, the greater the risk of acquiring disease from it.

The lifecycle of blacklegged ticks (Ixodes scapularis and Ixodes pacificus) generally lasts two years. During this time, they go through four life stages: egg, six-legged larva, eight-legged nymph, and adult. After the eggs hatch, the ticks must have a blood meal at every stage to survive.

Blacklegged ticks can feed from mammals, birds, reptiles, and amphibians. The ticks need to have a new host at each stage of their life, as shown below:

www.cdc.gov

Impact of air temperature variation on the ixod >

N. Tokarevich

a Laboratory of Zoonoses, St Petersburg Pasteur Institute, St Petersburg, Russia

b Scientific Research Center for Ecological Safety, Russian Academy of Sciences, St Petersburg, Russia

c Center for Hygiene and Epidemiology of Komi Republic, Syktyvkar, Russia

d Institute of Forecasting, Russian Academy of Sciences, Moscow, Russia

a Laboratory of Zoonoses, St Petersburg Pasteur Institute, St Petersburg, Russia

B. Evengard

e University Hospital, Umea University, Umea, Sweden

Background: The causes of the recent rise of tick-borne encephalitis (TBE) incidence in Europe are discussed. Our objective was to estimate the impact of air temperature change on TBE incidence in the European part of the Russian Arctic.

Methods: We analysed the TBE incidence in the Komi Republic (RK) over a 42-year period in relation to changes in local annual average air temperature, air temperature during the season of tick activity, tick abundance, TBE-prevalence in ticks, tick-bite incidence rate, and normalised difference vegetation index within the area under study.

Results: In 1998–2011 in RK a substantial growth of TBE virus (TBEV) prevalence both in questing and feeding ticks was observed. In 1992–2011 there was 23-fold growth of the tick-bite incidence rate in humans, a northward shift of the reported tick bites, and the season of tick bites increased from 4 to 6 months. In 1998–2011 there was more than 6-fold growth of average annual TBE incidence compared with 1970–1983 and 1984–1997 periods. This resulted both from the northward shift of TBE, and its growth in the south. In our view it was related to local climate change as both the average annual air temperature, and the air temperature during the tick activity season grew substantially. We revealed in RK a strong correlation between the change in the air temperature and that in TBE incidence. The satellite data showed NDVI growth within RK, i.e. alteration of the local ecosystem under the influence of climate change.

Conclusions: The rise in TBE incidence in RK is related considerably to the expansion of the range of Ixodes persulcatus. The territory with reported TBE cases also expanded northward. Climate change is an important driver of TBE incidence rate growth.

Introduction

Tick-borne infections are an increasing burden on healthcare in many countries. In the EU in 2012 tick-borne encephalitis (TBE) was included in the list of notifiable diseases,[1] and since then it is notifiable in 17 European countries.[2] In some regions of northern Europe there has been an uptrend in TBE cases.[3–6]

Immediate causes of TBE incidence growth and the distribution of Ixodidae ticks, the main vector of TBE virus (TBEV), are still not understood and depend on a number of factors,[7–12] the impact of climate change being one of them.[13–15]

TBE incidence depends on a number of factors, air temperature being one of them. Therefore it is necessary to study the impact of air temperature at the boundary of the region inhabited by TBE vectors (ixodid ticks), as both air temperature and TBE incidence have increased in recent years in the north of European Russia.

Earlier we have shown that the increase in average annual air temperature and “effective” temperature (in the period of tick activity) has a significant impact on the northward expansion of ixodid ticks and the rise in TBE incidence in Arkhangelsk Oblast of Russia.[16] Our studies revealed also that within the same period local precipitations varied very slightly and provided no significant impact on the ecology of ticks. In this regard, one may assume that events in Komi Republic (RK), neighbouring Arkhangelsk Oblast, may be influenced by the same climatic factors. Indeed, there has been a rise in TBE incidence and tick-bite incidence rates in RK ( Figure 1 ). However, “the association between those ups and changing climatic conditions require additional research and observation” (p. 50).[17] Therefore, as part of an international collaboration on effects of climate change on the spread of infectious diseases in the north (Clinf) we designed a study where we made use of RK official statistics, geographic and demographic data published by Russian Federation Federal State Statistic Service [see Rosstat http://www.gks.ru/], climatic, satellite-provided data for the analysis of vegetation change over time, and ecological and epidemiological data.

TBE incidence rate in Russia and in RK.

RK consists of 20 administrative units: 19 rural districts and one city district (Syktyvkar); however, Syktyvkar inhabitants mostly acquired TBEV in the adjacent Syktyvdinsk district, and for the ease of data processing we considered those two units together. About 95% of RK territory is taiga, and 5% tundra. For the purpose of this study 19 districts were divided into four geographic zones: Polar zone (polar tundra and tundra forest belt); Northern zone (boreal taiga), Central zone (middle taiga), Southern zone (southern taiga) ( Figure 2 ).

Komi Republic in the Russian Federation. Cutaway: administrative districts by zones. Southern zone: 1, Priluzskiy (S1); 2, Koigorodskiy (S2). Central zone: 3, Sysolskiy (C3); 4, Syktyvdinskiy + Syktyvkar city (C4); 5, Korterosskiy (C5); 6, Ust-Kulomskiy (C6); 7, Ust-Vymskiy (C7). Northern zone: 8, Udorskiy (N8); 9, Knyajpogostskiy (N9); 10, Ukhtinskiy (N10); 11, Sosnogorskiy (N11); 12, Troitsko-Pechorskiy (N12); 13, Vuktylskiy (N13). Polar zone: 14, Ust-Tsilemskiy (P14); 15, Ijemskiy (P15); 16, Pechorskiy (P16); 17, Usinskiy (P17); 18, Intinskiy (P18); 19, Vorkutinskiy (P19).

The RK population was 926,800 (1 January 2011), including the native Komi population, and minor indigenous ethnic groups: Khanty, Mansi and Nenets. Between 1970 and 2011 the RK population decreased by 4%.

Most of the Komi territory is covered by taiga (about 89%), with the far north-east occupied by tundra (2%). Other vegetation is represented by intermediate forms, swamps and meadows. Around 32,800 km 2 of mostly boreal forest (as well as some alpine tundra and meadows) in the Republic’s Northern Ural Mountains have been recognised in 1995 as a UNESCO World Heritage site, Virgin Komi Forests. It is the first natural UNESCO World Heritage site in Russia and the largest expanse of virgin forests in Europe. Siberian spruce, Scots pine and birch are widespread in this area.

The climate of RK is cold continental, subarctic, class “Dfc” by the Köppen climate classification.[18] Annual air temperature from 1970 to 2013 is about −1.3°С. Total precipitation is in the range of 600–700 mm per year, evaporation is about 200–300 mm per year, so the climate is humid with more precipitation than evaporation.

Materials and methods

Environmental and ep >The information used in our assessment of TBE situation in RK was as follows.

The monthly data on tick abundance (ticks per flag per hour) were calculated starting from the collection of ticks flagged (flannel flag sized 1.0 × 0.6 m) from vegetation in S1, S2, C3, C4, C6 administrative districts (see Figure 2 ) from May to July (I. persulcatus activity season) in 1970–1971, 1974–1980, 1982–1984, 1986–1992, 2000–2003, 2005–2011). Ticks were gathered in dull calm days when the air temperature was 12–18°С, and humidity 70–90%. Every 5 min ticks were removed from the flag with a surgical forceps, placed individually into a glass vial, and delivered to the laboratory the same day.

The standard method [19] was applied for tick species identification.

The collected ticks were tested for TBEV using enzymoimmunoassay (Vecto VKE-IgG manufactured by Vector-best, Novosibirsk, Russia).

The number of RK inhabitants seeking medical care after tick bites in 1992–2011 was considered. The background information including date and place of the event was provided to Russian Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing (Rospotrebnadzor) by medical institutions of each RK district, and the tick-bite incidence rate (TBIR), i.e. number of tick victims per 100,000 of population, was calculated as follows:

where N tv is number of tick victims within the district under study during the year, and р is the number of the district inhabitants.

TBE incidence rate in 1970–2011 was calculated as follows:

where IR TBE is TBE incidence rate, N TBE is the number of TBE cases within the district under study during the year, and р is the number of the district inhabitants.

TBE was diagnosed on the basis of clinical and epimediological data, and usually (97.3%) confirmed by seroprevalence study of paired sera in the dynamics of infectious process with certified diagnostic preparations.

Our study covered only cases of tick bites and/or TBEV infection occurring within RK territory, the criterion being the production of evidence that the patient had not left the district of residence at least 1 month prior to the event. In Russia, as in the former Soviet Union, health education firmly stressed that a person should rapidly seek healthcare after tick bite. The tick was then analysed for TBE and Borrelia burgdorferi. Specific immunoglobulin was offered if the tick contained TBEV. This explains the high number of persons with tick bites seeking healthcare.

Meteorological data

Meteorological data (air temperature in 1960–2013) were obtained from two main sources: National Climatic Data Center, USA (http://www.ncdc.noaa.gov/) and the Russian World Data Center for Meteorology (http://www.meteo.ru/), the data being collected at 10 meteorological stations in RK ( Table 1 ). Two types of database products were used: monthly-averaged and daily-averaged air temperatures. To calculate the effective temperatures we used data on mean daily temperatures reported by three stations: Koigorodok (Southern zone), Troicko-Pecherskoe (Northern zone), and Syktyvkar (Central zone).

RK meteorological stations.

Name
WMO number Latitude Longitude RK zone Date range, years
Vorkuta 23226 67°29′N 64°01′E Polar 1973–2013
Petrun’ 23324 66°26′N 60°46′E Polar 1960–2013
Ust’-Usa 23412 65°58′N 56°55′E Polar 1960–2013
Ust’-Cil’Ma 23405 65°26′N 52°10′E Polar 1900–2013
Pechora 23418 65°07′N 57°06′E Polar 1960–2013
Troicko-Pecherskoe 23711 62°42′N 56°12′E Northern 1900–2013
Uhta 23606 63°34′N 53°43′E Northern 1973–2013
Ust’-Kulom 23803 61°41′N 53°41′E Central 1973–2013
Syktyvkar 23804 61°40′N 50°51′E Central 1900–2013
Koigorodok 23904 60°26′N 50°58′E Southern 1960–2013

The average annual air temperature (AAAT) was calculated from the average monthly values reported by each station.

where Tij is monthly average air temperature on station j in month i. This way AAATj for all station were obtained. The AAAT values for Polar, Northern, Central, Southern zones, and for RK as a whole were defined as the average of AAAT values reported by the stations of the corresponding zone.

Satellite data

The normalised difference vegetation index (NDVI) derived from satellite-provided data was used to assess the change in vegetation during the period under study.[20]

where VIS and NIR are the spectral reflectance measurements acquired by satellite sensors in the visible (red) and near-infrared regions, respectively. Calculations of NDVI for a given point result in a number that ranges from minus one to plus one. However, lack of vegetation gives a value close to zero or below. NDVI values close to +1 (0.8–0.9) indicates the highest possible density of green leaves.

Two satellite-based databases covering the time period from 1982 to 2010 ( Table 2 ) were used: NOAA (AVHRR) data in range 1982–2001 with spatial resolution 8 km,[21] and Terra (MODIS) data in range 2000–2010 with resolution of 0.05° (about 5 km for the Komi area) [https://lpdaac.usgs.gov/products/modis_products_table/mod13c1].

Databases used for NDVI assessment.

Satellite (instrument)
Data range, years Spatial resolution Database
NOAA (AVHRR) 1982–2001 8 km GIMMS (Global Inventory Modeling and Mapping Studies)
Terra (MODIS) 2000–2010 0.05° NASA Land Processes Distributed Active Archive Center, product MOD13C1

Statistical analysis

The primary statistical data processing resulted in values averaged over time intervals, and the standard deviations of the variables under study.

Pearson correlation analysis was performed to assess the correlation between the air temperature and TBE incidence.

where xi indicates values from dataset 1, …, xn> containing n values; yi indicates values from dataset 1, …, yn> containing n values; ẋ and ẏ are the sample mean for dataset x and analogously for y; δx and δy are the standard deviation of x and y respectively. Microsoft Excel was used for correlation assessment (Microsoft).

Regression analysis was applied to determine the AAAT that triggers TBE incidence growth. It was conducted to evaluate the statistical significance of the results. Microsoft Excel was used for regression analysis.

The sum of effective temperatures reflects the amount of heat necessary for full development of all stages of Ixodes persulcatus in its season of activity, and was calculated by the formula [22,23]:

where S is the annual sum of effective temperatures; ETn = (tn – tmin) indicates effective temperature at day n; tmin is temperature limit, °С (+10°С for Ixodes persulcatus); and tn is day “n” average temperature, °С (only if tn > tmin).

Tick species, abundance, and TBE prevalence

The maximal abundance of ixodid ticks was registered in July. To determine the dominant species 241 ticks at random were examined, of which 225 (93.4 ± 1.6%) proved to be Ixodes persulcatus. In July according to long-term observations the tick abundance in the Southern zone (S1, S2) was 2.3–3.2 ticks (imago) per flag per hour, and in the Central zone (С3, C4, C6) it was 0.2 ( Table 3 ).

Geographical coordinates of sites where ticks were flagged.

Latitude, N
Longitude, E
S1 (Priluzskiy) 60°7′46″–60°41′6″ 48°43′51″–49°42′49″
S2 (Koigorodskiy) 60°26′43″–60°40′8″ 50°21′20″–50°59′59″
C3 (Sysolskiy) 60°50′49″–61°5′12″ 49°38′17″–50°20′21″
C4 (Syktyvdinskiy + Syktyvkar city) 61°9′29″–61°57′7″ 50°10′42″–50°50′9″
C6 (Ust-Kulomskiy) 61°15′33″–61°48′48″ 53°10′56″–53°51′40″

In 1998–2008 in Southern and Central zones (S1, S2, C3, and C4) 133 questing ticks flagged from plantation were tested, and TBEV was found in none of them.

In 2009–2011 in the same sites 285 ticks were flagged and tested, and 27 (9.5%) proved to be TBEV-positive.

In 1998–2008, 1,968 feeding ticks were collected from humans and domestic animals (dogs and cats). In average 6.3 ± 4.5% of those ticks were TBEV-positive. TBEV-positive ticks belonged to collections from eight districts: S1, S2, C3, C4, C5, C6, C7 and N9.

In 2009–2011, within the same districts, 4,080 feeding ticks were collected from humans and domestic animals; TBEV-prevalence in them was higher: 11.0 ± 1.6% (p-value 0.016) ( Table 4 ).

TBE virus prevalence in ticks removed from humans and domestic animals in 1998–2008 and in 2009–2011.

RK district
Positive /studied (%)
1998–2008 2009–2011
N9 3/53 (5.7%) 13/129 (10.1%)
С7 4/76 (5.2%) 20/193 (10,3%)
С6 19/210 (9.1%) 30/310 (9.7%)
С5 7/137 (5.1%) 21/210 (10.0%)
С4 35/656 (5.3%) 159/1296 (12.3%)
C3 27/433 (6.2%) 94/894 (10.5%)
S2 9/126 (7.1%) 27/290 (9.3%)
S1 20/277(7.2%) 94/758 (12.4%)
Total 124/1968 (6.3%) 449/4080 (11.0%)

Tick bite inc >In 1992–2011 in RK there was 23-fold increase in number of patients seeking medical care because of tick bites: from 103 in 1992 to 2,369 in 2011.

In 1992–2001 TBIR was 23, while in 2002–2011 it reached 110. The most pronounced increase in TBIR, up to 228, was observed in 2009–2011.

The boundary of territory with recorded tick bites shifted northward considerably ( Figure 3 , Table 5 ). In 1992–1993 tick bites occurred only in Southern (S1, S2), and Central districts (C3, C4), but in 2006–2011 they were recorded in all RK districts, except for P14.

TBIR (tiсk bite incidence rate) in RK districts in 1992–2001, and in 2002–2011.

RK district
1992–2000 2001–2011
P19 0.00 0.16
P18 0.00 0.45
P17 0.00 1.07
P16 0.00 1.60
P15 0.00 1.84
P14 0.00 0.00
N13 0.00 6.59
N12 0.00 25.42
N11 0.00 4.77
N10 0.00 6.66
N9 5.38 69.01
N8 0.00 11.77
C7 14.04 181.04
C6 32.79 221.29
C5 30.89 154.26
C4 20.75 101.09
C3 188.34 1071.08
S2 272.47 1024.07
S1 326.49 1185.50

Tick bite incidence rate in RK districts in 1992–2001, and in 2002–2011.

The season of tick activity extended from 4 to 6 months: in 1992–2001 tick bites occurred from May to August, while in 2011 they were recorded from April to September.

Most of those tick bites occurred during recreation time in the forest (51.7%), allotment gardens (33.6%), parks or cemeteries (8.9%); only 5.8% of tick bites occurred during working time or at an unknown place ( Table 6 ).

Places of tick bites in RK.

Place of tick bite
Tick bite incidence
Number of tick-bitten humans %
Recreation areas, forests 3,114 51.7
Allotment gardens 2,023 33.6
Parks or cemeteries 536 8.9
Work areas or unknown areas 349 5.8
Total 6,023 100

TBE inc >For clarity of presentation the analysed 42-year time range (1970–2011) was divided into three 14-years periods: I: 1970–1983, II: 1984–1997, and III: 1998–2011.

In 1970–2011 135 TBE cases were reported in RK. There was a clearly increasing trend of TBE incidence ( Figures 1 and ​ and4, 4 , Table 7 ). Thus, the average annual TBE incidence rate was virtually the same in periods I (0.12) and II (0.11), but underwent a 6-fold increase in period III (0.74), and grew dramatically in 2009–2011 (2.17). This trend was opposite to the decreasing trend in Russia as a whole within the same time periods. ( Table 8 )

TBE incidence rate in RK districts for three 14-year periods

RK district
1970–1983 1984–1997 1998–2011
P19 0.00 0.08 0.00
P18 0.00 0.00 0.00
P17 0.00 0.00 0.00
P16 0.00 0.09 0.09
P15 0.00 0.00 0.00
P14 0.00 0.00 0.00
N13 0.00 0.26 0.27
N12 0.00 0.00 0.00
N11 0.00 0.00 0.14
N10 0.00 0.00 0.06
N9 0.00 0.00 0.31
N8 0.00 0.41 0.00
C7 0.00 0.00 0.36
C6 0.00 0.00 2.84
C5 0.00 0.00 0.00
C4 0.00 0.00 0.59
C3 0.00 0.00 4.32
S2 0.59 6.11 9.84
S1 3.20 1.74 14.66

TBE incidence rate in RK and in whole Russia

Time period
TBE incidence rate in RK TBE incidence rate in Russia
1970–1983 0.12 1.24
1984–1997 0.11 3.46
1998–2011 0.74 3.38
2009–2011 2.17 2.43

TBE incidence rate in RK districts for 14-year periods: 1, 0.0–0.099; 2, 0.1–0.99; 3, 1.0–4.99; 4, > 5.0.

The boundary of territory with recorded TBE cases moved northward considerably in recent years. During Period I TBE cases occurred only in RK Southern zone (S1, S2), during Period II in Southern (S1, S2) and Northern (N8, N13) zones, and in Period III in all zones (S1, S2, C3, C4, C6, C7, N9, N11, N13). A few TBE cases occurred even in N10, and P16. The sharp TBE incidence rise in RK resulted both from a northward shift of TBE cases and from their more frequent occurrence in Central and, especially, Southern zones ( Figure 4 ).

Changes in temperature and TBE inc >In 1970–1989 in RK the AAAT ranged from −3.5°C to +0.9°C, and averaged −1.6°C. In 1990–1999 AAAT was −1.35°C on average in the same range from −3.5°C to +0.9°C.

After 2000 AAAT in RK increased gradually and never fell below −2.2°C. In 2000–2011 AAAT was −0.7°C in range of −2.2°C to +0.8°C, i.e. exceeded the level of 1970–1989 by 0.9°C. TBE incidence rate increased with AAAT ( Figure 5 ).

AAAT and TBE incidence rate in RK.

In the Southern zone AAAT ( Figure 6 ) increased from +0.9°C (1970–1989) to +2.0°C (2000–2011). The TBE incidence rate remained low in the 1980s, but it started growing after 1990 to reach 38 in 2010).

AAAT and TBE incidence rate in Southern (top) and Central (bottom) zones of RK.

Within the same period in the Central zone AAAT ( Figure 6 ) increased from +0.5 to +1.5°C. Here the TBE incidence rate steadily rose after the end of the 1990s and exceeded 5 by 2010.

In the Northern zone in 1970–1989 AAAT was −0.7°C, but in 2000–2011 it reached +0.1°C. Only sporadic TBE cases were reported here during the entire analysed period.

To reveal the dependence of the TBE incidence rate on climate change we considered the longest series of meteorological data ( Table 1 ). AAAT was calculated and its averaging was performed by the moving-average method with a 9-year window. So the long series of meteorological observations allowed us to properly compare the averaged air temperatures with TBE incidence rates also averaged with a 9-year window.

The comparison ( Figure 7 ) demonstrated that the significant increase in AAAT between 1989 and 1995 resulted in a rise of TBE incidence rate to 0.25. The second period of AAAT growth that started in 2000 resulted in a dramatic, up to 1.5, increase in the TBE incidence rate.

AAAT and TBE incidence in RK averaged with 9-year window. The blue arrows show the periods of sharp rise in the air temperature.

The sum of effective temperature trends ( Figure 8 ) calculated for the 14-year periods revealed significant increment in the sum of effective temperatures between 1970 and 2000: it increased by 213°C in the Southern zone, by 183°C in the Central zone, and by 168°C in the Northern zone.

Annual sums of effective temperatures averaged over 14-year periods for Northern, Central, and Southern zones of RK, and annual average TBE incidence rate for RK.

An analysis of the relationship between the changes in AAAT and TBE incidence rate within each RK zone ( Table 9 ) shows high probability of a strong correlation coefficient between them in the whole RK 0.77 (p Figure 9 ). It was shown that the set of data may be divided as follows: a stagnation region when AAAT rose from 0.75 to 1.2°C but did not result in TBE incidence growth, and its rate ranges from 0.54 to 1.65. But when AAAT exceeded 1.4°C, there was a dramatic rise in TBE incidence rate up to 16.

The regressional analysis of TBE incidence rate and AAAT in RK Southern zone in 1970–2011. Both AAATs and TBE incidence rates are averaged with 9-year window. The dash line shows the linear trend. “A”-balloon displays the stagnation period (low AAAT, low TBE incidence rate), “B”-balloon displays the uptrend in AAAT and TBE incidence rate.

The local NDVI dynamics correspond to AAAT changes and shows a definite increase of vegetation index from 1980s to 2000s ( Figure 10 ). Thus, NDVI in RK increased from 0.36 (in 1980s) to 0.39 (1990s–2000s) when AAAT ran up from −1.57°C to −0.83°C.

The variations in NDVI and AAAT in RK. Dash lines show linear trends in NDVI and AAAT.

Discussion

In the second half of the twentieth century significant changes in biotic components of the ecosystems occurred in the European North of Russia. There was some northward expansion of forested area, most probably due to climatic changes,[24–26] that caused northward distribution of many species of wild mammals, which are the main tick vectors.

NDVI has been shown to be a good predictor to forecast the abundance of I. ricinus.[27] In RK NDVI increased with AAAT and confirmed that changes in the local ecosystem improved significantly the life conditions for ixodid ticks over the period under study. Furthermore, in the Arctic region, including the north of Russia, there is an increasing trend in the incidence of some zoonotic diseases not related to ticks.[28,29]

To estimate the changes in tick habitats we analysed TBIR data over 20-year period in different RK districts.

In 1992–1993 it was only in Southern and Central zones (five districts) that people sought medical care after tick bites, however, in 2002–2011 this happened in most RK districts, including those of Northern and Polar zones, even over 65 N°. The same type of health information was given in all zones. Forty years ago the northern boundary of the tick habitat was much closer to the south,[30] but now in RK it has shifted northward by 150–200 km.[31]

The removal of ticks by healthcare providers from residents of Northern and Polar zones who had not travelled out of their district for a at least month, proves that ixodid tick habitat covers now almost the entire territory of RK.

To some extent, the presented data support the assessment of climate-related changes in the range of I. persulcatus calculated with the help of simple empirical models linking the possibility of formation a sustainable habitat of ticks to environment temperature and precipitations.[32]

We consider the influence of temperature as a main driving factor of the northward tick expansion in Komi. As the climate of the research area is humid (more precipitation than evaporation) water content does not prevent the spreading of ticks. The distribution of precipitation in Komi is uniform over the year, and there is no dry season.

Tick distribution in new areas, extension of timespan of tick bites, and increase of TBEV prevalence in ticks provide a background for the uptrend in TBE incidence. The northward expansion of tick habitat and TBIR increase are nearly synchronous with the rise in TBE incidence rate and, especially, with that in new territories. This proves that transmission is the main pathway of TBE infection in the RK population. The sharp rise in TBE incidence rate in RK is due both to significant northward shift of the infection and to its considerable increase in the south. Climate change is an important driver of those phenomena. A strong correlation is established between AAAT and TBE incidence rate in Southern, Central and Northern zones and in the whole RK. The correlation degree increases southward, thus indicating that the most pronounced changes both in AAAT and in TBE incidence rate occurred in RK Southern zone synchronously.

The effective temperature governs the duration of the different stages of tick life cycle. The ability of ticks to lay eggs and hatch in one season depends on the sum of effective temperatures.[7,33,34] Complete development of I. persulcatus requires a sum of effective temperatures no less than 1,400°C over the period, with a stable average temperature exceeding 10°C.[23] This is only a rough figure only, because with minimal heat provision survival of ticks depends largely on the topography of the land.

In 1970–1997 during the season of tick activity in Southern and Central zones of RK the heat supply only slightly exceeded the critical level (+1.25°C), and did not reach it within Northern zone. In 1998–2011 in Southern, Central, and Northern zones heat supply increased significantly to compare with the earlier period, and in the Northern zone it exceeded the minimal level needed for tick survival. Increased heat supply has improved the life conditions in new territories, resulting in the northward distribution of blood-sucking arthropods.

The northward distribution of ticks due to the increase in air temperature also took place in other north European countries,[35,36] and in the Czech Republic, where TBE-infected ticks were found in the mountains much higher than previously. TBE cases started to occur in those areas.[37–39]

It should be underlined that all above-mentioned studies deal with the spread of TBE by I. ricinus. The distinctive feature of our study that it was conducted in the area where I. persulcatus dominates. This species is significantly different from I. ricinus by its biological characteristics, e.g. due to its much higher cold resistance, so its habitat stretches much to north. Moreover, TBEV prevalence in I. persulcatus is usually considerably higher than that in I. ricinus.[40]

The increasing trend in TBE prevalence in I. persulcatus, as revealed in recent years both in questing (flagged) and feeding (on humans and animals) ticks, should be considered as a factor that may have an impact on TBE incidence rate in RK. Moreover, the territory with TBE-infected ticks expanded to the north.

The rise by a few degrees in mean air temperature resulted in a 200–1,000 km northward shift of tick habitat boundaries in Canada.[41]

A sharp rise in TBE incidence caused by the northward distribution of ticks due to climate change had been registered in Arkhangelsk region neighbouring RK,[16] confirming the assumed significant influence of climate change on TBE incidence in the Northern European part of Russia, where there is a boundary of I. persulcatus habitat. However, in other Russian regions located further to the south, with permanent abundance of ticks, a rise in AAAT does not trigger TBE incidence growth.[42] This probably means that in localities with temperatures sufficient for ticks some other drivers govern the incidence more.

As it was already mentioned above, climate change in the Northern European part of Russia not only improves the life conditions for I. persulcatus, but influences its hosts significantly, providing more favourable conditions for their distribution in new territories. Of course, the higher AAAT may have an impact on the local human population as well, as they spend more time outdoors. This may also increase the probability of exposure to tick bites.[6]

There may be some other factors, apart from climate change, that may have a synergistic effect on the increase in TBE incidence. Evaluation of their roles requires a special investigation.

However, the frequently cited arguments that socio-economic factors,[43–45] increasing awareness of the health authorities [46] or more frequent contacts with ticks due to large-scale agricultural activities [12] contribute to the TBE incidence rise are not particularly applicable in the case of RK.

First of all, the economic trends in RK do not differ from those in other Russian regions. Moreover, in terms of average income per capita, in 2010 RK occupied a rather high place (12th of 80) among the subjects of the Russian Federation, and its ranking was stable for many years.[47]

Secondly, it would be difficult to explain why TBE diagnostics improved recently only in RK, as the all-Russia TBE incidence rate tended to decline. Third, the vast majority of tick bites in RK occurred in leisure time, in parks, gardens or forests, and were not related to production activities. Also, the RK population decreased during the period under study.

The northward distribution of ticks in Northern Europe is a new formidable challenge for the healthcare of northern countries. The severity of the situation is increased by a number of circumstances. Firstly, the majority of I. persulcatus ticks in RK are infected with TBEV of Far East genotype, known for its high mortality rate.[48] We cannot exclude the possibility of distribution of this TBE genotype to other countries, e.g. by migrant birds.[49, 50]

Secondly, in the Northern European Russia I. persulcatus ticks are infected not only with TBE, but with some other pathogens that cause dangerous diseases.[51–53]

Third, the indigenous population, previously never exposed to tick bites, may be more susceptible to tick-borne infections than the population in RK Southern zone.[15]

These findings show that it is important to improve the prevention of tick-borne infections among local population, especially indigenous Arctic ethnic groups never previously exposed to ticks.

Conclusions

The northward expansion of the I. persulcatus range in the Russian Arctic and, particularly, in RK is demonstrated.

The reason for this expansion was significant increase both in the average annual air temperature and the sum of effective temperatures that define satisfactory temperature conditions for I. persulcatus egg-laying and hatching during one season.

Using satellite-provided data it was established that over the past decades in the Russian Arctic, including RK, significant changes in ecosystems took place that improved the life conditions for ixodid ticks.

The marked rise in the TBE incidence rate in RK is largely associated with the expansion of the range of I. persulcatus. The territory with recorded TBE cases expanded northward significantly. Climate change is an important driver of the increase in TBE incidence.

The occurrence of TBE cases in new territories justifies the need to update TBE-preventive measures in current conditions, taking into account the protection of indigenous Arctic ethnic groups.

Funding Statement

This work was supported by NordForsk.

Disclosure statement

No potential conflict of interest was reported by the authors.

www.ncbi.nlm.nih.gov

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