Literature DB >> 31002047

Rickettsiales in Ticks Removed from Outdoor Workers, Southwest Georgia and Northwest Florida, USA.

Elizabeth R Gleim, L Mike Conner, Galina E Zemtsova, Michael L Levin, Pamela Wong, Madeleine A Pfaff, Michael J Yabsley.   

Abstract

We determined the prevalence of selected Rickettsiales in 362 ticks removed from outdoor workers in southwest Georgia and northwest Florida, USA. Persons submitted an average of 1.1 ticks/month. We found Ehrlichia chaffeensis in an Amblyomma maculatum tick, and Panola Mountain Ehrlichia sp. in 2 A. maculatum ticks and 1 Dermacentor variabilis tick.

Entities:  

Keywords:  Ehrlichia; Florida; Georgia; Rickettsia; Rickettsiales; United States; outdoor workers; tick bites; tickborne infections; ticks; vectorborne infections; zoonoses

Mesh:

Year:  2019        PMID: 31002047      PMCID: PMC6478216          DOI: 10.3201/eid2505.180438

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


The southeastern United States has multiple tick species that can transmit pathogens to humans. The most common tick species, Amblyomma americanum, is the vector for the causative agents of human ehrlichioses and southern tick-associated rash illness, among others (). Dermacentor variabilis ticks can transmit the causative agent of Rocky Mountain spotted fever, and Ixodes scapularis ticks can transmit the causative agents of Lyme disease, babesiosis, and human granulocytic anaplasmosis (). Although less common in the region, A. maculatum ticks are dominant in specific habitats and can transmit the causative agent of Rickettsia parkeri rickettsiosis (). Persons who have occupations that require them to be outside on a regular basis might have a greater risk for acquiring a tickborne disease (). Although numerous studies have been conducted regarding risks for tickborne diseases among forestry workers in Europe, few studies have been performed in the United States (,). The studies that have been conducted in the United States have focused on forestry workers in the northeastern region (). However, because of variable phenology and densities of ticks, it is useful to evaluate tick activity and pathogen prevalence in various regions and ecosystems. Burn-tolerant and burn-dependent ecosystems, such as pine (Pinus spp.) and mixed pine forests commonly found in the southeastern United States, have unique tick dynamics compared with those of other habitats (). The objective of this study was to determine the tick bite risk and tickborne pathogen prevalence in ticks removed from forestry workers working in pine and mixed pine forests in southwest Georgia and northwest Florida, USA. During June 2009–December 2011, forestry workers in southwestern Georgia (7 counties) and northwestern Florida (1 county) submitted ticks crawling on or attached to them. We identified ticks and tested them for selected pathogens (Appendix). Immature forms of the same species from the same day and person were pooled (<5 nymphs and <20 larvae) for testing. A total of 53 persons submitted 362 ticks (Table). Excluding larvae, the most common tick species submitted was A. maculatum, followed by A. americanum, I. scapularis, and D. variabilis. On 4 occasions, 1 person submitted A. tuberculatum ticks (3 batches of larvae and 1 batch of nymphs) from a longleaf pine site in Baker County, Georgia. Average submissions per persons were 2.6 ticks (median 1 tick), but 1 person submitted 100 ticks. A total of 24 persons submitted ticks more than once, and they submitted an average of 0.08–6.5 ticks/month (overall average submission rate of 1.1 ticks/month). Three ticks were engorged (1 D. variabilis adult, 1 A. americanum nymph, and 1 Amblyomma sp. nymph); only the Amblyomma sp. nymph was positive for a pathogen (R. amblyommatis).
Table

Prevalence of Ehrlichia chaffeensis, PME, and Rickettsia spp. in ticks submitted by outdoor workers, southwestern Georgia and northwestern Florida, USA*

Tick species and stageMonths submittedNo. positive ticks/no. tested (%)
Rickettsia spp.†
E. chaffeensis PMERickettsia spp.
Amblyomma americanum, adultsFeb–Sep0/11 (0)0/11 (0)4/11 (36.4)2 R. amblyommatis
A. americanum nymphs‡Mar–Sep0/43 (0)0/43 (0)12/43 (27.9)9 R. amblyommatis
A. americanum larvae‡Apr and Oct0/5 (0)0/5 (0)1/5 (20.0)1 R.amblyommatis
Amblyomma sp. nymphsJun and Oct0/3 (0)0/3 (0)1/3 (33.3)1 R. amblyommatis§
Amblyomma sp. larvaeOct0/5 (0)0/5 (0)0/5 (0)
A. maculatum adultsMay–Oct1/83 (1.2)2/83 (2.4)¶18/83 (21.7)5 R. amblyommatis,§ 
4 R. parkeri,§ 1 Rickettsia sp. TR-39/TX125, 2 Candidatus R. andeanae
A. tuberculatum nymphs‡Apr0/5 (0)0/5 (0)1/5 (5.0)1 novel SFG Rickettsia sp.
A. tuberculatum larvae‡Feb#0/182 (0)0/182 (0)10/182 (5.5)**10 novel SFG Rickettsia sp.**
Dermacentor variabilis adultsJun–Aug0/10 (0)1/10 (10.0)2/10 (20.0)1 R. amblyommatis§
Ixodes scapularis adultsOct–MarNT0/15 (0)7/15 (46.7)4 Rickettsia sp. TR-39, 3 R. buchneri

*All Rickettsia spp. were identified by sequencing unless otherwise noted. NT, not tested; PME, Panola Mountain Ehrlichia sp., SFG, spotted fever group.
†Rickettsia spp. for whom amplicons did not provide high-quality bidirectional sequences were categorized as unknown Rickettsia spp.
‡Minimum infection prevalence is no. positive tick pools/no. ticks tested.
§The following R. amblyommatis samples were identified by restriction fragment length polymorphism analysis: for 1 D. variabilis adult, 5 A. maculatum adults, and 1 Amblyomma sp. nymph; for A. americanum, 1 adult, 2 nymphs, and 1 larva. Three A. maculatum adults were also identified as containing R. parkeri positive by restriction fragment length polymorphism analysis.
¶Data included in Loftis et al. ().
#Date was known only for 1 submission of 20 larvae. Dates for others were not provided when submitted.
**Data included in Zemtsova et al. ().

*All Rickettsia spp. were identified by sequencing unless otherwise noted. NT, not tested; PME, Panola Mountain Ehrlichia sp., SFG, spotted fever group.
†Rickettsia spp. for whom amplicons did not provide high-quality bidirectional sequences were categorized as unknown Rickettsia spp.
‡Minimum infection prevalence is no. positive tick pools/no. ticks tested.
§The following R. amblyommatis samples were identified by restriction fragment length polymorphism analysis: for 1 D. variabilis adult, 5 A. maculatum adults, and 1 Amblyomma sp. nymph; for A. americanum, 1 adult, 2 nymphs, and 1 larva. Three A. maculatum adults were also identified as containing R. parkeri positive by restriction fragment length polymorphism analysis.
¶Data included in Loftis et al. ().
#Date was known only for 1 submission of 20 larvae. Dates for others were not provided when submitted.
**Data included in Zemtsova et al. (). Rickettsia spp. prevalence was 36.4% in adult, 27.9% in nymphal, and 20% in larval A. americanum ticks; R. amblyommatis was the only species identified (Table). Rickettsia spp. were detected in 23% of A. maculatum adults; R. amblyommatis was most common (6.0%), followed by R. parkeri (4.8%). A previously detected novel Rickettsia sp. was identified in 10 of 11 A. tuberculatum larval pools and was reported by Zemtsova et al. (). An additional pool of A. tuberculatum nymphs was tested in this study and also was positive for the novel Rickettsia sp. E. chaffeensis was detected in 1 A. maculatum adult (prevalence 1.2%), and Panola mountain Ehrlichia sp. was detected in 2 A. maculatum adults (prevalence 2.4%) and 1 D. variabilis adult (prevalence 10%). No ticks were positive for Borrelia spp., E. ewingii, or Anaplasma phagocytophilum. Thus, forestry workers were found to encounter ticks on a regular basis, and peak encounter rates reflected previously reported tick seasonality in this region (). Only 3 (0.8%) of the ticks submitted were engorged, indicating prompt removal of most ticks and thus low risk for pathogen transmission. A. maculatum, a fairly uncommon tick in the southeastern United States, was the most commonly submitted tick. However, A. maculatum ticks dominate in regularly burned pine ecosystems (), which is where most of these workers spent their time. We observed several unique findings related to pathogens during this study. Larvae and nymphs of A. tuberculatum ticks were submitted on multiple occasions, a tick rarely reported on humans (). These findings in conjunction with the identification of a novel Rickettsia sp. (), suggest that additional research is warranted. This study also identified E. chaffeensis and Panola Mountain Ehrlichia in A. maculatum ticks. Although A. americanum ticks are considered the primary vector of Ehrlichia spp., these pathogens have been occasionally reported in questing A. maculatum ticks, suggesting that this tick might be involved in their transmission cycles (,). We also detected Panola Mountain Ehrlichia in 1 D. variabilis tick. Thus, further research regarding these alternative tick species as potential vectors of these pathogens is warranted, particularly in the case of A. maculatum ticks, which were a common species on forestry workers and are widespread in this region ().

Appendix

Additional information on Rickettsiales in ticks removed from outdoor workers, southwest Georgia and northwest Florida, USA.
  8 in total

1.  Infectious disease occurrence in forestry workers: a systematic review.

Authors:  Douglas J Covert; Ricky L Langley
Journal:  J Agromedicine       Date:  2002       Impact factor: 1.675

2.  Evaluation of Gulf Coast Ticks (Acari: Ixodidae) for Ehrlichia and Anaplasma Species.

Authors:  Michelle E J Allerdice; Joy A Hecht; Sandor E Karpathy; Christopher D Paddock
Journal:  J Med Entomol       Date:  2017-03-01       Impact factor: 2.278

3.  Detection of a novel spotted fever group Rickettsia in the gophertortoise tick.

Authors:  Galina E Zemtsova; Elizabeth Gleim; Michael J Yabsley; L Mike Conner; Tom Mann; Mary D Brown; Lori Wendland; Michael L Levin
Journal:  J Med Entomol       Date:  2012-05       Impact factor: 2.278

4.  A ten-year study of tick biting in Mississippi: implications for human disease transmission.

Authors:  Jerome Goddard
Journal:  J Agromedicine       Date:  2002       Impact factor: 1.675

5.  Panola Mountain Ehrlichia in Amblyomma maculatum From the United States and Amblyomma variegatum (Acari: Ixodidae) From the Caribbean and Africa.

Authors:  Amanda D Loftis; Patrick J Kelly; Christopher D Paddock; Keith Blount; Jason W Johnson; Elizabeth R Gleim; Michael J Yabsley; Michael L Levin; Lorenza Beati
Journal:  J Med Entomol       Date:  2016-01-07       Impact factor: 2.278

Review 6.  Beyond Lyme: aetiology of tick-borne human diseases with emphasis on the south-eastern United States.

Authors:  E Y Stromdahl; G J Hickling
Journal:  Zoonoses Public Health       Date:  2012-09       Impact factor: 2.702

7.  Prevalence of Rickettsiales in ticks removed from the skin of outdoor workers in North Carolina.

Authors:  Sangmi Lee; Madhavi L Kakumanu; Loganathan Ponnusamy; Meagan Vaughn; Sheana Funkhouser; Haley Thornton; Steven R Meshnick; Charles S Apperson
Journal:  Parasit Vectors       Date:  2014-12-23       Impact factor: 3.876

8.  The phenology of ticks and the effects of long-term prescribed burning on tick population dynamics in southwestern Georgia and northwestern Florida.

Authors:  Elizabeth R Gleim; L Mike Conner; Roy D Berghaus; Michael L Levin; Galina E Zemtsova; Michael J Yabsley
Journal:  PLoS One       Date:  2014-11-06       Impact factor: 3.240

  8 in total
  2 in total

1.  The Ixodes scapularis Symbiont Rickettsia buchneri Inhibits Growth of Pathogenic Rickettsiaceae in Tick Cells: Implications for Vector Competence.

Authors:  Benjamin Cull; Nicole Y Burkhardt; Xin-Ru Wang; Cody J Thorpe; Jonathan D Oliver; Timothy J Kurtti; Ulrike G Munderloh
Journal:  Front Vet Sci       Date:  2022-01-06

2.  Association between lone star tick bites and increased alpha-gal sensitization: evidence from a prospective cohort of outdoor workers.

Authors:  Cedar L Mitchell; Feng-Chang Lin; Meagan Vaughn; Charles S Apperson; Steven R Meshnick; Scott P Commins
Journal:  Parasit Vectors       Date:  2020-09-14       Impact factor: 3.876

  2 in total

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