Pitfalls in Tick and Tick-Borne Pathogens Research, Some Recommendations and a Call for Data Sharing
"> Figure 1
<p>The coexistence of different tick cohorts in monthly samples may result in a different response to weather variables. The figure shows a hypothetical pattern of tick activity, in which they may not be active in summer because of high evaporation, and in winter, because of low temperature or short photoperiod. “Monthly time intervals” refer to an undetermined period of time. Even though the example is hypothetical, it is inspired by the realized activity of <span class="html-italic">Ixodes</span> spp. in parts of the Holarctic region. Ticks, thus, have different patterns of recruitment. In spring, newly molted ticks after winter (light blue) mix with ticks that passed the winter in quiescence and regained activity (dark blue). As spring moves into summer, more newly molt ticks incorporate into the questing stage, and old ticks from the previous year die or find a host. After the summer, ticks molt in spring (light blue) regain activity and young ticks (dark blue) result from molts. At the end of the autumn, ticks questing since spring have already most likely died or found a host, and most ticks may come from the molt after summer. Therefore, ticks of different physiological ages coexist in the same month and are collected together. This affects the modeling of the “response” of ticks to weather and enhances the need to provide raw data for weather with every report to allow reliable future meta-analyses. Created with BioRender.com.</p> "> Figure 2
<p>The scheme shows a Gaussian-type distribution of a species of tick on a population of hosts, with every host carrying ticks and a variable number of ticks on each host, and a negative binomial distribution, showing how most ticks are concentrated on a few hosts, while most hosts do not carry ticks at all. Both distributions are displayed as a chart. Mean number of ticks and standard deviation are the same for both distributions. Created with BioRender.com.</p> "> Figure 3
<p>The effect of tick sampling on hosts on the determination of the Minimum Infection Rate (MIR) of a hypothetical pathogen. In table A we introduce four hypothetical host specimens (A, B, C, D) that carry 10, 20, 30 or 40 ticks. Of these hosts, researchers can retrieve all or a fraction of these ticks (indicated in the columns) and pools are prepared assuming a fixed number of 5 ticks per pool. We also assumed a fixed positivity rate of 50% under every condition, and made assumptions about the ways the calculation of MIR is affected by these factors. The chart shows the values of MIR obtained from hosts A, B, C or D based on the number of positive pools. It can be observed that values can change from MIR = 2.5 to MIR = 10 according to the number of ticks collected, assuming the same infection rate. The conclusion is two-fold: even if researchers consider MIR from ticks collected while feeding to be reliable (which it is not), it is deeply affected by the number of ticks collected. Created with BioRender.com.</p> "> Figure 4
<p>The inaccuracies commonly reported when estimating the Minimum Infection Rate (MIR) of a pathogen detected in ticks collected while feeding. In (<b>A</b>), ticks are collected from different species of hosts and pooled together. We believe that unreliable conclusions would be drawn from these data, since there is no way to determine which host (if any) contributed to the presence of pathogen-derived DNA in the feeding ticks. In (<b>B</b>), ticks are collected from the same species of host, but only one host is contributing to the presence of the pathogen; pools contain material from different individuals. If pools are random, ticks coming from the only positive host could “contaminate” every sample giving an overestimate of the infection rate in ticks. In (<b>C</b>), the most commonly reported situation, the infection status of vertebrates is not recorded. We recommend not to use MIR values based on collections of feeding ticks. These data may demonstrate the presence of a pathogen in a site but should never be used in a quantitative way. Created with BioRender.com.</p> ">
Abstract
:1. Introduction
2. Surveying Off-Host Ticks
2.1. How Ticks Respond to Environmental Variables
2.2. The Challenges of Field Collections
2.2.1. The Repeatability of the Measurements of Tick Density
2.2.2. The Evaluation of the Physiological Stage of a Tick
2.2.3. Proposals for Weather Recording
2.2.4. The Systematic Description of the Vegetation in Which Surveys Were Carried Out
2.2.5. Other Issues Associated with Collections of Off-Hosts Ticks
3. The Reporting of Prevalence of Ticks on Hosts
4. The Reporting of Prevalence of Pathogens in Ticks
4.1. Reporting Pathogen Prevalence in Questing Ticks
- Pools must contain only the same species and stage of ticks.
- A method like the Minimum Infection Rate (MIR) [33] can be used to assess the prevalence if working with pools.
- Individual details of each pool or individual ticks should be included in a supplementary file attached to the publication, to provide context.
4.2. Reporting Tick-Borne Pathogens in Feeding Ticks
5. GenBank, the Molecular Identification of Ticks and the Bona Fide Sequences
- a.
- Representative tick specimens even when not describing new species, should be made available, if possible. These specimens should be deposited in a widely acknowledged international tick collection, facilitating the exchange of material. The voucher specimens could then be examined in case of concerns with the sequence(s) obtained from them. The DNA extraction should be done ensuring maintenance of the specimen in the best possible condition, avoiding the loss of morphological structures of interest. The DNA can be extracted (i) from a single leg leaving the rest of the specimen intact or (ii) making a cut in the lateral third of the idiosome and collecting the exoskeleton after incubation and lysis of tissues.
- b.
- The search for downloadable sequences in GenBank is not a random selection. Researchers should use sequences coming from (i) type or neotype specimens of (re)descriptions of species and with voucher specimens available, (ii) specimens for which a complete gene has been sequenced, to obtain more phylogenetic information, (iii) specimens for which reliable illustrations exist in the original publication allowing an unbiased identification of the tick in case of concerns. It would be necessary to mark these bona fide sequences as gold standards for future research.
- c.
- Always use the complete gene sequences. Do not use sequences from “species yet to be characterized” or that are striking records far from the known range of the target species. This is not a rejection of these records, but a cautionary comment about their indiscriminate use before the data is firmly established as reliable.
- d.
- If available, include the geographical coordinates of the specimen when submitting sequences to GenBank. The name of a country alone associated with a sequence is insufficient for further meta-analysis. Phylogeographical studies could be developed if coordinates are included, associating sequences with other factors that could drive the disparity observed in the tree. This is something yet unexplored in many fields of ticks and transmitted pathogens research, despite the increasing number of sequences with coordinates. The preferred method, other than submission to international repositories, would be to publish the sequence as supplementary material to placing it in context with the contents, findings, and available data.
6. Evidence for Vectorial Competence of Ticks
- Null evidence: detection of pathogen DNA/RNA in a fed tick (or a pool) retrieved from hosts; these data only create noise in the corpus of research. Records could be used for reporting presence/absence of a pathogen in a site (i.e., using the ticks as “sentinels”). Its support for further conclusions is null.
- Spatial overlap of vector, vertebrate and pathogen distributions: there is a statistical association of the spatial distribution of the three actors. For example, the distribution of Cytauxzoon felis in the USA overlaps the known distribution of the tick Amblyomma americanum and the host, the bobcat (Lynx rufus) [48]. The association is statistical, demonstrating that prevalence was significantly higher in sites with established populations of A. americanum. Collectively, these data suggest that the bobcat is a natural host for C. felis and that A. americanum is likely a prominent vector.
- Presence of a single tick species associated with a high prevalence of a pathogen in a host population (or in high loads relative to other species): this may be indicative of a tick circulating the pathogen to the hosts, but also that the tick acquired the pathogen while feeding on other hosts in previous stages of its life cycle. Results should be interpreted with caution. For example, a high prevalence of a Hepatozoon felis-like strain in a grey fox (Lycalopex griseus) population in Argentinian Patagonia was reported [49], and Amblyomma tigrinum was the only tick species found on those foxes. Thus, a potential role of A. tigrinum as a vector of Hepatozoon is suggested, with further evidence needed to confirm this.
- Detection of pathogen DNA/RNA in ticks retrieved from hosts, after bloodmeal digestion and molting: this is proof that at least remnants of the pathogen’s DNA/RNA persist in the tick after molting. It is not a clear demonstration that the complete and infective pathogen is still in the tick after molting but warrants future studies on the system.
- Detection of pathogen in tick salivary glands: the pathogen managed to survive the molting instar and migrate to salivary glands of the tick. This is an indication that the system deserves special attention.
- Observation of mature parasite stages in the tick (i.e., the sporogonic development of some Hepatozoon sp.). For example, evidence has been provided of sporogonic development of Hepatozoon canis in specimens of (reported as) Rhipicephalus turanicus ticks collected from a naturally infected fox from southern Italy [50]. In the case of some Hepatozoon sp., the tick must be ingested by the host to complete the cycle. Therefore, in ticks (definitive host) the cycle is completed when gamont develops, reproduces sexually, and matures into sporozoites.
- Full evidence: Experimental assay involving infected vertebrates feeding naïve ticks, detection of the pathogen in fed and molted ticks, allowing these newly infected ticks to feed in naïve vertebrates and detection of the pathogen in the latter. This has also been referred to as “xenodiagnosis”. This is final proof of the circulation of a pathogen by a tick. However, a contrasting view is that “what happens in the laboratory, does not necessarily happen in nature”. The establishment of vectorial ability must be ideally based on both laboratory and epidemiological evidence [51].
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Appendix A. Definitions
- Aggregated (Negative binomial) distribution: a distribution of parasites or pathogens in which few individuals host high burdens, whereas most individuals host few or no parasites.
- Cohort: a group of ticks that moult and quest in the same period of time and therefore have a similar physiological age.
- Data logger: a device that measures and records data (e.g., temperature and humidity) at defined intervals.
- Gaussian distribution: a distribution following a bell-shaped curve with an equal number of measurements above and below the mean value. It is also known as Normal distribution.
- Minimum Infection Rate: the ratio of the number of positive pools to the total number of ticks (or other vectors) tested for a given pathogen (abbreviated as MIR).
- Poisson distribution: a probability distribution that expresses the probability of a given number of events occurring in a fixed interval of time or space if these events occur with a known constant mean rate and independently of the time since the last event.
- Physiological age: the environmental stress that a tick has supported since its last molt (or hatching); it is directly related to their energy reserves and how they are depleted. It commonly depends on accumulated temperature and accumulated saturation deficit, two variables that can be easily measured with data loggers.
- Phytosociology: a botanical discipline that describes the diversity of plant communities and the environment of a given territory, in terms of associations of plants. It is a hierarchical definition of vegetal species that tend to appear together because of climate gradients and soil conditions. It is extensively used in Europe and provides an unbiased classification of the cohort of vegetal species occurring together. For example, the Tilio-Acerion is “an alliance of sub-montane maple and lime woods of humid ravines from among the mixed broadleaf woodlands of more fertile soils. It typically has a diverse canopy of trees and a rich ground flora of herbs, ferns and bryophytes dependent on nutrient-rich moist soils”. The meaning of the i.e., the alliance “Pegano-Harmalae-Salsoletea Vermiculatae” may be hard to capture by tick researchers, but it is defined as “Thermomediterranean and Macaronesian halo-nitrophilous semidesert scrub” with several subcategories, which immediately has an ecological meaning for tick research (references are included in the main body of the text of the manuscript).
- Questing (or host-seeking): a behaviour of most hard ticks consisting of waiting on the vegetation to meet a host.
- Voucher specimen: a tick specimen from which a molecular sequence was obtained that is kept in a collection, and freely loaned to researchers who want to examine it. This is mainly carried out to compare the morphology of the voucher specimen with other specimens and to conciliate both morphological and molecular identifications.
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Estrada-Peña, A.; Cevidanes, A.; Sprong, H.; Millán, J. Pitfalls in Tick and Tick-Borne Pathogens Research, Some Recommendations and a Call for Data Sharing. Pathogens 2021, 10, 712. https://doi.org/10.3390/pathogens10060712
Estrada-Peña A, Cevidanes A, Sprong H, Millán J. Pitfalls in Tick and Tick-Borne Pathogens Research, Some Recommendations and a Call for Data Sharing. Pathogens. 2021; 10(6):712. https://doi.org/10.3390/pathogens10060712
Chicago/Turabian StyleEstrada-Peña, Agustín, Aitor Cevidanes, Hein Sprong, and Javier Millán. 2021. "Pitfalls in Tick and Tick-Borne Pathogens Research, Some Recommendations and a Call for Data Sharing" Pathogens 10, no. 6: 712. https://doi.org/10.3390/pathogens10060712