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¹ Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, USA
² Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, Georgia 30602, USA
³ Viral and Rickettsial Zoonoses Branch, Centers for Disease Control and Prevention, Atlanta, Georgia 30333, USA
⁴ Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, Oklahoma 74078, USA
⁵ Corresponding author (email: myabsley{at}uga.edu)

	ABSTRACT

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ABSTRACT:   An Ehrlichia sp. (Panola Mountain [PM] Ehrlichia sp.) closely related to Ehrlichia ruminantium was recently detected in a domestic goat experimentally infested with lone star ticks (LSTs, Amblyomma americanum) collected from Georgia, USA. The infected goat exhibited pyrexia and mild clinical pathologic abnormalities consistent with ehrlichiosis. At least two other Ehrlichia species (Ehrlichia chaffeensis and Ehrlichia ewingii) are maintained in nature by a cycle involving LSTs as the primary vector and white-tailed deer (Odocoileus virginanus) as a known or suspected reservoir. To investigate the possibility that white-tailed deer are potential hosts of the PM Ehrlichia sp., whole blood samples collected from 87 wild deer from 2000 to 2002 were screened with a species-specific nested PCR assay targeting the citrate synthase gene. In addition, two laboratory-raised white-tailed deer fawns were each infested with 120 wild-caught LST adults from Missouri, USA, and blood samples were periodically collected and tested for the PM Ehrlichia sp. Of 87 deer tested from 20 locations in the southeastern United States, three (3%) deer from Arkansas, North Carolina, and Virginia were positive for the PM Ehrlichia sp. Wild-caught ticks transmitted the PM Ehrlichia sp. to one of two deer fawns, and colony-reared nymphal LSTs acquired the organism from the deer, maintained it transstadially as they molted to adults, and transmitted the PM Ehrlichia sp. to two naïve fawns. These findings indicate that white-tailed deer are naturally and experimentally susceptible to infection with an Ehrlichia sp. closely related to E. ruminantium and are able to serve as a source of infection to LSTs.
  Key words:  Amblyomma, cervid, Cowdria, Ehrlichia chaffeensis, Ehrlichia ruminantium, heartwater, lone star tick.

	INTRODUCTION

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Ehrlichia spp. are a group of tick-transmitted, intracellular, Gram-negative bacteria that cause disease in a wide range of hosts, including humans, domestic dogs, ruminants, equids, and felids (Rikihisa, 1991). Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis, is maintained in a cycle involving white-tailed deer (WTD; Odocoileus virginianus) as a primary reservoir and the lone star tick (LST; Amblyomma americanum) as a primary vector (Ewing et al., 1995; Lockhart et al., 1997a, b; Yabsley et al., 2003). Field evidence and experimental infection trials also suggest that WTD are important hosts for at least two other LST-vectored organisms, Ehrlichia ewingii and Borrelia. lonestari, and natural infections of WTD with all three organisms have been reported in much of the range of the LST (Lockhart et al., 1997a; Yabsley et al., 2002; Arens et al., 2003; Moore et al., 2003; Moyer et al., 2006).

Ehrlichia ruminantium, previously Cowdria ruminantium, the causative agent of heartwater (cowdriosis) in ruminants, is widely distributed in sub-Saharan Africa and is established on some islands in the Caribbean (Deem, 1998). Numerous species of Amblyomma ticks can transmit E. ruminantium, but Amblyomma variegatum and Amblyomma hebraeum are the two primary vectors in Africa. There is great concern that, were E. ruminantium introduced into the United States, the organism could readily establish in wildlife reservoirs and native ticks. White-tailed deer are experimentally susceptible to infection with E. ruminantium (Dardiri et al., 1987), and the Gulf Coast, USA, tick, Amblyomma maculatum, has been experimentally shown to be a competent vector (Mahan et al., 2000). In addition, E. ruminantium has recently been recognized as a zoonotic disease in South Africa (Allsopp et al., 2005).

Recently an Ehrlichia sp. (Panola Mountain [PM] Ehrlichia sp.) closely related to E. ruminantium was detected in LSTs from Panola Mountain State Park in Georgia, USA (Loftis et al., 2006). The organism was detected in a domestic goat that was experimentally infested with wild-caught LSTs. This goat developed pyrexia and clinical pathologic changes consistent with ehrlichiosis (monocytosis, neutropenia with increased lymphocytes, decreased alkaline phosphatase activity). The DNA of the PM Ehrlichia sp. was detected in blood samples collected on days post–tick exposure (DPTE) 19, 21, and 34. Antibodies cross-reactive with E. chaffeensis were detected in serum samples, with a maximum titer of 256 on DPTE 38. Laboratory-raised LST nymphs acquired the PM Ehrlichia sp. from the goat and transstadially maintained the infection (Loftis et al., 2006). Recently the PM Ehrlichia sp. was detected via polymerase chain reaction (PCR) in a blood sample from a human patient from Atlanta, Georgia, with a history of a LST bite, fever, and muscle pain that resolved after treatment with doxycycline (Reeves et al., unpubl. data).

Because the PM Ehrlichia sp. is suspected to be transmitted by LSTs, and because WTD are susceptible to infection with three other LST-vectored organisms (Lockhart et al., 1997a, b; Yabsley et al., 2002; Moore et al., 2003; Yabsley et al., 2003), we hypothesized that WTD might be natural hosts for the PM Ehrlichia sp. In this study, we conducted a PCR-based survey of WTD blood samples collected from WTD populations with known exposure to LST-vectored organisms. In addition, we infected WTD with the PM Ehrlichia sp. by transmission-feeding wild-caught LSTs from Missouri, USA, on two laboratory-raised WTD fawns, and we evaluated their ability to infect colony-reared nymphal LSTs.

	MATERIALS AND METHODS

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From 2000 to 2002, whole blood samples from 87 deer from 20 sites (Table 1) in the southeastern United States with known exposure to A. americanum–transmitted organisms were collected in Vacutainer EDTA tubes and frozen at –20 C until PCR testing. For PCR, DNA was extracted from 200 µl of whole blood using the GFX Genomic Blood Purification kit (Amersham Pharmacia Biotech, Piscataway, New Jersey, USA) according to the manufacturer’s instructions. To detect the PM Ehrlichia sp., a nested PCR protocol for the citrate synthase gene (~433 bp) (Loftis et al., 2008) was conducted using the external primers Ehr3CS–185F (5'-GCCAC-CGCAGATAGTTAGGGA) and Ehr3CS–777R (5'-TTCGTGCTCGTGGATCATAGTTTT) in a 25 µl reaction that contained 11 µl molecular biology-grade water, 2.5 µl 25 mM MgCl₂, 5 µl 5X colorless buffer (Promega, Madison, Wisconsin, USA), 0.25 µl 20 mM dNTPs (Promega), 0.5 µl of each primer (50 µM), 0.25 µl GoTaq^® Flexi polymerase (Promega), and 5 µl of sample DNA. For the nested PCR, 1 µl of primary product was used as template in a 25 µl reaction containing the same PCR components except primers Ehr3CS–214F (5'-TGTCATTTCCACAGCATTCTCATC) and Ehr3CS–619R (5'-TGAGCTGGTCCCCA-CAAAGTT) (Loftis et al., 2008). Cycling conditions in both the primary and secondary reactions were 40 cycles of 94 C for 30 sec, 55 C for 30 sec, and 72 C for 30 sec. This protocol has a sensitivity of 10 gene copies as determined by PCR with a cloned plasmid containing the gltA gene from the Ehrlichia sp. (Loftis et al., 2008).

Two 6-mo-old, laboratory-reared white-tailed deer fawns (ID nos. 12 and 18) were housed in a tick-proof facility for the duration of these experiments. Before experimental exposure to A. americanum, both fawns were negative for antibodies reactive to E. chaffeensis and PCR-negative for E. chaffeensis, E. ewingii, the PM Ehrlichia sp., A. phagocytophilum, the Anaplasma sp. of WTD, and Borrelia spp. Adult A. americanum wild-caught in Missouri (n=120 per fawn) were placed in tick chambers secured in a mid-lateral position on each deer fawn. Whole blood samples were collected on DPTE 3, 7, 14, 24, 27, 29, 31, 34, 42, 49, and 56 and tested for DNA of the PM Ehrlichia sp. by PCR as described above. At DPTE 27, laboratory-raised A. americanum nymphs from Oklahoma State University (n=200 per deer) were fed on fawns 12 and 18. Replete nymphs from both deer fawns were collected, pooled, allowed to molt, and a subset of resulting adults (n=20) was individually dissected, all internal organs were removed and digested overnight in SDS/ proteinase K, and nucleic acid was isolated by standard phenol/chloroform extraction followed by ethanol precipitation (Sambrook et al., 1989). Water controls were included during each extraction process. Resultant pellets were dissolved in 100 µl of molecular biology-grade water, and 5 µl were used in nested PCR for the PM Ehrlichia sp. as previously described. At necropsy, samples of skin, inguinal lymph node, mesenteric lymph node, spleen, kidney, bone marrow, lung, liver, and ear were collected from both deer and processed for routine histopathology and PCR testing for the PM Ehrlichia sp. as described above. For DNA extraction, tissues (~5 mg) were digested with proteinase K and extracted using the GFX extraction kit.

Remaining molted adult ticks that were acquisition fed as nymphs (n=120) were divided randomly into two pools of 60 ticks each and allowed to feed on two naïve deer fawns (ID numbers 8 and 32). Blood samples were collected from each deer every 3–4 days for 56 days post-transmission feeding and evaluated for evidence of infection. At necropsy, the same organs, plus the brain, were collected and processed as described for fawns 12 and 18.

	RESULTS

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The PM Ehrlichia sp. was detected in three of 87 (3%) deer from the southeastern United States by nested PCR (Table 1). A single 1-yr-old deer was coin-fected with the PM Ehrlichia sp. and E. ewingii, and the two remaining PM Ehrlichia-positive deer (both 1.5-yr-old) were coinfected with E. chaffeensis. Sequence analysis of gltA amplicons from two deer were 100% identical to the PM Ehrlichia sp. detected in an experimentally infected goat (GenBank DQ363995) and from A. americanum from numerous southeastern states (Loftis et al., 2008). One gltA amplicon from a wild deer had a single polymorphic base (nucleotide 289 AR as numbered by DQ363995).

One of the two deer fawns (no. 18) experimentally infested with wild-caught adult A. americanum became PCR positive for the PM Ehrlichia sp. on DPTE 24 and was positive until DPTE 42. The gltA sequence of the PM Ehrlichia sp. from deer fawn 18 was 100% identical to GenBank no. DQ363995. The second fawn (no. 12) was PCR negative for the PM Ehrlichia sp. on all sampling dates. Eight of 20 (40%) adult LSTs that had been fed as nymphs on the two deer fawns were PCR positive for the PM Ehrlichia sp. Fawns 8 and 32, who each received 60 adult LSTs acquisition fed as nymphs, both became PCR positive for the PM Ehrlichia sp. by DPI 24 and 27, respectively, and one fawn remained PCR positive until DPI 52 (Table 2). At necropsy, samples of both of the lymph nodes that were examined, lung, and bone marrow were PCR positive for the PM Ehrlichia sp. (Table 2). No histopathologic lesions were noted in any deer fawns.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Because of the association of the PM Ehrlichia sp. and LSTs, we tested only deer populations with known exposure to LSTs and evidence of infection with other LST-vectored organisms. Coinfections of humans and domestic animals with multiple pathogens transmitted by the same vector are being increasingly recognized (Sexton et al., 1998; Kordick et al., 1999; Loebermann et al., 2006), as are coinfected individual ticks (Schulze et al., 2005; Mixson et al., 2006). These reports of coinfection resulted from infestations with single or limited numbers of ticks that are coinfected; because WTD are frequently infested with hundreds to thousands of LSTs, the likelihood of coinfection in wild WTD is increased (reported as high as 25%) (Yabsley et al., 2002, 2003; Arens et al., 2003; Moore et al., 2003). In the current study, all three wild deer that were positive for the PM Ehrlichia sp. also were infected with either E. chaffeensis or E. ewingii. Coinfection of individual WTD with E. chaffeensis/E. ewingii, E. chaffeensis/B. lonestari, and E. ewingii/B. lonestari has been detected in previous studies (Yabsley et al., 2002; Arens et al., 2003). Infestation of deer fawns with as few as 300 wild-caught A. americanum resulted in coinfection with E. chaffeensis, E. ewingii, and B. lonestari (Varela-Stokes, 2007). The majority of WTD that are PCR positive for E. chaffeensis, E. ewingii, and B. lonestari are 1.5 yr old (Lockhart et al., 1997b; Yabsley et al., 2002; Moore et al., 2003; Yabsley et al., 2003); a similar association with age was observed with the PM Ehrlichia sp.

WTD are highly susceptible to experimental infection with E. ruminantium and display significant morbidity and mortality (Dardiri et al., 1987). However, the PM Ehrlichia sp. did not cause mortality in the three experimentally infected deer. No health data were available for the three hunter-killed wild deer. Although one of our experimentally infected fawns did develop pyrexia, mild anemia, and depression concomitant with development of PM Ehrlichia sp. infection, simultaneous co-infection with a Theileria sp. and E. chaffeensis precluded accurate interpretation of serology or hemograms (Little et al., unpubl. data). Future work will be aimed at the in vitro isolation of the PM Ehrlichia sp. so that experimental infection and transmission trials can be conducted in monospecifically infected hosts.

Data from this study and others demonstrate that WTD are exposed to at least five ehrlichial species (E. chaffeensis, E. ewingii, PM Ehrlichia sp., Anaplasma phagocytophilum, and Anaplasma sp. of WTD) (Dawson et al., 1996; Belongia et al., 1997; Lockhart et al., 1997a; Yabsley et al., 2002, 2003; Arens et al., 2003; Moore et al., 2003). Four of these species are known to be zoonotic, and WTD have been shown to be competent reservoirs of E. chaffeensis and PM Ehrlichia sp. Because of the reported low level of serologic cross-reactivity between E. chaffeensis and the PM Ehrlichia sp. in goats (Loftis et al., 2006), it is possible that low-titer E. chaffeensis seroreactors in prior studies of WTD actually represent infection with the PM Ehrlichia sp, E. chaffeensis, E. ewingii, or mixed infections. The presence of multiple, serologically cross-reactive ehrlichiae also raises the possibility that prior infection of WTD with E. chaffeensis or other ehrlichiae could confound serologic surveys for E. ruminantium, should it be introduced into the United States. Future studies should utilize an array of diagnostic assays for epidemiologic studies, and experimental infections should investigate coinfection dynamics.

	ACKNOWLEDGMENTS

 
The authors thank M. Savage, S. Adams, D. Hurst, M. West, K. Allen, and the Animal Resources staff at Oklahoma State University for assistance with fawn care, and L. Parsons for excellent technical assistance. We also thank D. Osborne and personnel at GA DNR for assistance in obtaining fawns. This research was supported in part by 1R56AI062834-01A1 from the National Institutes of Health; Cooperative Agreement 2001-96130032-CA, Veterinary Services, APHIS, USDA; Cooperative Agreement 01ERAG0013, United States Geological Survey, Biological Resources Division, USDI; and sponsorship of SCWDS by the fish and wildlife agencies of Alabama, Arkansas, Florida, Georgia, Kentucky, Kansas, Louisiana, Maryland, Mississippi, Missouri, North Carolina, Ohio, Puerto Rico, South Carolina, Tennessee, Virginia, and West Virginia, USA. Support from the states to SCWDS was provided in part by the Federal Aid to Wildlife Restoration Act (50 Stat. 917).

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
ALLSOPP, M. T., M. LOUW, AND E. C. MEYER. 2005. Ehrlichia ruminantium: An emerging human pathogen. South African Medical Journal 95: 541.[Medline]

ARENS, M. Q., A. M. LIDDELL, G. BUENING, M. GAUDREAULT-KEENER, J. W. SUMNER, J. A. COMER, R. S. BULLER, AND G. A. STORCH. 2003. Detection of Ehrlichia spp. in the blood of wild white-tailed deer in Missouri by PCR assay and serologic analysis. Journal of Clinical Microbiology 41: 1263–1265.[Abstract/Free Full Text]

BELONGIA, E. A., K. D. REED, P. D. MITCHELL, C. P. KOLBERT, D. H. PERSING, J. S. GILL, AND J. J. KAZMIERCZAK. 1997. Prevalence of granulocytic Ehrlichia infection among white-tailed deer in Wisconsin. Journal of Clinical Microbiology 35: 1465–1468.[Abstract/Free Full Text]

DARDIRI, A. H., L. L. LOGAN, AND C. A. MEBUS. 1987. Susceptibility of white-tailed deer to experimental heartwater infections. Journal of Wildlife Diseases 23: 215–219.[Abstract/Free Full Text]

DAWSON, J. E., C. K. WARNER, V. BAKER, S. A. EWING, D. E. STALLKNECHT, W. R. DAVIDSON, A. A. KOCAN, J. M. LOCKHART, AND J. G. OLSON. 1996. Ehrlichia-like 16S rDNA sequence from wild white-tailed deer (Odocoileus virginianus). Journal of Parasitology 82: 52–58.[Medline]

DEEM, S. L. 1998. A review of heartwater and the threat of introduction of Cowdria ruminantium and Amblyomma spp. ticks to the American mainland. Journal of Zoo and Wildlife Medicine 29: 109–113.[Medline]

EWING, S. A., J. E. DAWSON, A. A. KOCAN, R. W. BARKER, C. K. WARNER, R. J. PANCIERA, J. C. FOX, K. M. KOCAN, AND E. F. BLOUIN. 1995. Experimental transmission of Ehrlichia chaffeensis (Rickettsiales: Ehrlichieae) among white-tailed deer by Amblyomma americanum (Acari: Ixodidae). Journal of Medical Entomology 32: 368–374.[Medline]

KORDICK, S. K., E. B. BREITSCHWERDT, B. C. HEGARTY, K. L. SOUTHWICK, C. M. COLITZ, S. I. HANCOCK, J. M. BRADLEY, R. RUMBOUGH, J. T. MCPHERSON, AND J. N. MACCORMACK. 1999. Coinfection with multiple tick-borne pathogens in a Walker Hound kennel in North Carolina. Journal of Clinical Microbiology 37: 2631–2638.[Abstract/Free Full Text]

LOCKHART, J. M., W. R. DAVIDSON, D. E. STALL-KNECHT, J. E. DAWSON, AND E. W. HOWERTH. 1997a. Isolation of Ehrlichia chaffeensis from wild white-tailed deer (Odocoileus virginianus) confirms their role as natural reservoir hosts. Journal of Clinical Microbiology 35: 1681–1686.[Abstract/Free Full Text]

———, ———, ———, ———, AND S. E. LITTLE. 1997b. Natural history of Ehrlichia chaffeensis (Rickettsiales: Ehrlichieae) in the Piedmont physiographic province of Georgia. Journal of Parasitology 83: 887–894.[Medline]

LOEBERMANN, M., V. FINGERLE, M. LADEMANN, C. FRITZSCHE, AND E. C. REISINGER. 2006. Borrelia burgdorferi and Anaplasma phagocytophilum coinfection. Emerging Infectious Diseases 12: 353–355.[Medline]

LOFTIS, A. D., W. K. REEVES, J. P. SPURLOCK, S. M. MAHAN, D. R. TROUGHTON, G. A. DASH, AND M. L. LEVIN. 2006. Infection of a goat with a tick-transmitted Ehrlichia from Georgia, U.S.A., that is closely related to Ehrlichia ruminantium. Journal of Vector Ecology 31: 213–222.[Medline]

———, T. R. MIXSON, E. Y. STROMDAL, M. J. YABSLEY, L. E. GARRISON, P. C. WILLIAMSON, R. R. FITAK, P. E. FUERST, D. J. KELLY, AND K. W. BLOUNT. 2008. Geographic distribution and genetic diversity of the Ehrlichia sp. from Panola Mountain in Amblyoma americanum. BMC Infectious Diseases 8: In press.

MAHAN, S. M., T. F. PETER, B. H. SIMBI, K. KOCAN, E. CAMUS, A. F. BARBET, AND M. J. BURRIDGE. 2000. Comparison of efficacy of American and African Amblyomma ticks as vectors of heartwater (Cowdria ruminantium) infection by molecular analyses and transmission trials. Journal of Parasitology 86: 44–49.[Medline]

MIXSON, T. R., S. R. CAMPBELL, J. S. GILL, H. S. GINSBERG, M. V. REICHARD, T. L. SCHULZE, AND G. A. DASCH. 2006. Prevalence of Ehrlichia, Borrelia, and Rickettsial agents in Amblyomma americanum (Acari: Ixodidae) collected from nine states. Journal of Medical Entomology 43: 1261–1268.[Medline]

MOORE, V. A., A. S. VARELA, M. J. YABSLEY, W. R. DAVIDSON, AND S. E. LITTLE. 2003. Detection of Borrelia lonestari, putative agent of southern tick-associated rash illness, in white-tailed deer (Odocoileus virginianus) from the southeastern United States. Journal of Clinical Microbiology 41: 424–427.[Abstract/Free Full Text]

MOYER, P. L., A. S. VARELA, M. P. LUTTRELL, V. A. MOORE IV, D. E. STALLKNECHT, AND S. E. LITTLE. 2006. White-tailed deer (Odocoileus virginianus) develop spirochetemia following experimental infection with Borrelia lonestari. Veterinary Microbiology 115: 229–236.[Medline]

RIKIHISA, Y. 1991. The tribe Ehrlichiae and ehrlichial diseases. Clinical Microbiology Reviews 4: 286–308.[Abstract/Free Full Text]

SAMBROOK, T. L., E. F. FRITSCH, AND T. MANIATIS. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, New York, 1,659 pp.

SCHULZE, T. L., R. A. JORDAN, C. J. SCHULZE, T. MIXSON, AND M. PAPERO. 2005. Relative encounter frequencies and prevalence of selected Borrelia, Ehrlichia, and Anaplasma infections in Amblyomma americanum and Ixodes scapularis (Acari:Ixodidae) ticks from central New Jersey. Journal of Medical Entomology 42: 450–456.[Medline]

SEXTON, D. J., G. R. COREY, C. CARPENTER, L. Q. KONG, T. GANDHI, E. BREITSCHWERDT, B. HEGARTY, S. M. CHEN, H. M. FENG, X. J. YU, J. OLANO, D. H. WALKER, AND S. J. DUMLER. 1998. Dual infection with Ehrlichia chaffeensis and a spotted fever group rickettsia: A case report. Emerging Infectious Diseases 4: 311–316.[Medline]

VARELA-STOKES, A. S. 2007. Transmission of bacterial agents from lone star ticks to white-tailed deer. Journal of Medical Entomology 44: 478–483.[Medline]

YABSLEY, M. J., A. S. VARELA, C. M. TATE, V. G. DUGAN, D. E. STALLKNECHT, S. E. LITTLE, AND W. R. DAVIDSON. 2002. Ehrlichia ewingii infection in white-tailed deer (Odocoileus virginianus). Emerging Infectious Diseases 8: 668–671.[Medline]

———, V. G. DUGAN, D. E. STALLKNECHT, S. E. LITTLE, J. M. LOCKHART, J. E. DAWSON, AND W. D. DAVIDSON. 2003. Evaluation of a prototype Ehrlichia chaffeensis surveillance system using white-tailed deer (Odocoileus virginianus) as natural sentinels. Vector Borne and Zoonotic Diseases 3: 195–207.

Received for publication 23 March 2007.

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Yabsley, M. J. Articles by Little, S. E. Search for Related Content PubMed PubMed Citation Articles by Yabsley, M. J. Articles by Little, S. E.