<<

Veterinary Parasitology 228 (2016) 17–22

Contents lists available at ScienceDirect

Veterinary Parasitology

journal homepage: www.elsevier.com/locate/vetpar

Research paper

Ectoparasites of free-roaming domestic in the central United States

a b,1 a a,∗

Jennifer E. Thomas , Lesa Staubus , Jaime L. Goolsby , Mason V. Reichard

a

Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, 250 McElroy Hall Stillwater, OK 74078, USA

b

Department of Clinical Science, Center for Veterinary Health Sciences, Oklahoma State University, 1 Boren Veterinary Medical Teaching Hospital

Stillwater, OK 74078, USA

a r t i c l e i n f o a b s t r a c t

Article history: Free-roaming domestic (Felis catus) populations serve as a valuable resource for studying ectoparasite

Received 11 May 2016

prevalence. While they share a similar environment as owned cats, free-roaming cats do not receive rou-

Received in revised form 27 July 2016

tine veterinary care or ectoparasiticide application, giving insight into parasite risks for owned .

Accepted 29 July 2016

We examined up to 673 infested cats presented to a trap-neuter-return (TNR) clinic in the central United

States. Ectoparasite prevalences on cats were as follows: fleas (71.6%), (18.7%), Felicola subrostratus

Keywords:

(1.0%), blakei (0.9%), and Otodectes cynotis (19.3%). Fleas, ticks, and O. cynotis were found in

Cat

all months sampled. A total of 1117 fleas were recovered from 322 infested cats. The predominate flea

Feline

recovered from cats was Ctenocephalides felis (97.2%) followed by Pulex spp. (2.8%), Cediopsylla simplex

Felis catus

(0.6%), and Nosopsyllus fasciatus (0.6%). A total of 373 ticks were recovered from 126 infested cats. The

Feral cat

Stray cat predominate was Amblyomma americanum (65.9%) followed by Ixodes scapularis (32.5%), Der-

Ectoparasite macentor variabilis (10.3%), and Rhipicephalus sanguineus (0.8%). Immature tick stages accounted for 54.7%

Flea of all ticks found, highlighting an under-appreciated source of tick burden on domestic cats. The results

Tick

of this study emphasize the importance of year-round use of ectoparasiticides with both insecticidal and

Louse

acaricidal activity on domestic cats.

Mite

© 2016 Elsevier B.V. All rights reserved.

Ear

1. Introduction have varying ectoparasiticide protocols, which may differ within a

shelter as well, depending on the individual ’s personality

Free-roaming domestic cat (Felis catus) populations serve as a and response to being handled. Shelter animals are obtained from

valuable resource for studying ectoparasite prevalence. Sometimes a variety of sources (i.e., owner surrender, confiscation, stray, or

called community cats, the term free-roaming can be employed feral) and have an unknown history of acaricide use and veterinary

to describe feral, stray, and other non-owned cats which are not care. Variations in shelter holding time prior to sampling also raises

considered and live exclusively outdoors (Centonze and Levy, the question of whether parasites were acquired prior to shelter

2002). Many of these cats have a close association with homes and acquisition or from contaminated shelter environments. Similarly,

human activities, sharing a similar environment as domestic pets. shelter surveys may underestimate the prevalence of tick infesta-

However, since these free-roaming domestic cats have limited or tions. Ticks feed for a period of 2–14 days (Diamant and Strickland,

no history of veterinary care or ectoparasiticide use, they provide a 1965) and may have fed to repletion and fallen off a host by the

unique sampling population to estimate risk of ectoparasite expo- time an animal is examined in a shelter survey. Thus, sampling free-

sure for owned cats under veterinary care. roaming domestic cats can provide unique insight into ectoparasite

Ectoparasite studies of free-roaming cats provide value over prevalence.

similarly conducted shelter surveys for multiple reasons. Shelters Historically, ectoparasite studies conducted on cats have pri-

marily focused on fleas. This is likely due to the number of

recognized flea-transmitted pathogens (i.e., Bartonella spp., Rick-

ettsia felis, Mycoplasma haemofelis, Dipylidium caninum, etc.) and

Corresponding author. relative ease of flea detection and collection in comparison to other

E-mail address: [email protected] (M.V. Reichard). ectoparasites. There are few primary literature reports of natu-

1

Present address: Department of Veterinary Technology, Oklahoma State Uni-

ral tick infestations on cats in the United States (Akucewich et al.,

versity, 230 Agriculture Resource Center, 400N, Portland Avenue, Oklahoma City,

2002; Bishopp and Trembley, 1945; Burroughs et al., 2016; Curran

OK 73107, USA.

http://dx.doi.org/10.1016/j.vetpar.2016.07.034

0304-4017/© 2016 Elsevier B.V. All rights reserved.

18 J.E. Thomas et al. / Veterinary Parasitology 228 (2016) 17–22

and Fish, 1989; Magnarelli et al., 1990; Shock et al., 2014) and 2.4. Ear

even fewer comprehensive ectoparasite surveys (Akucewich et al.,

2002). The purpose of the current study was to characterize the On each cat sampled, the vertical portion of the external ear

prevalence of a variety of ectoparasites in a free-roaming domes- canal was swabbed using cotton-tipped applicators regardless of

tic cat population presented to a trap-neuter-return clinic in the presence, color, or texture of exudate. Each swab was placed in an

central United States. individual vial until examination. Each swab was examined indi-

vidually using a stereomicroscope within 5 h of collection. Swab

surfaces were examined for all life stages of Otodectes cynotis.

2. Materials and methods

2.5. Data analyses

2.1. Feline population

The prevalence of ectoparasite infestation was calculated

Cats were sampled opportunistically from animals presented to

according to Bush et al. (Bush et al., 1997). 95% confidence inter-

a trap-neuter-return (TNR) clinic in north central Oklahoma, USA.

vals were calculated according to Sterne’s exact method (Reiczigel,

All cats were required to be a minimum of 3 months of age in order

2003) using Quantitative Parasitology 3.0 (Rózsa et al., 2000). Com-

to participate in the clinic. Any indication that a cat was owned, as

parisons of the prevalence of fleas, ticks, and ear mite among

determined by the presence of a collar or microchip, disqualified the

months sampled and age group of cats were done using Chi-square

cat from participation in the clinic and ectoparasite collection. All

(Sokal and Rohlf, 1997). Chi-square tests were performed using

research procedures and sample collections were approved by the

SigmaPlot 12.5 (Systat Software Inc., San Jose, California, United

Oklahoma State University Institution Animal Care and Use Com-

States). The prevalence of lice and fur mites were not compared

mittee (IACUC). Trappers signed a waiver permitting these samples

statistically due to the low occurrence of parasites. Statistical sig-

to be collected and data used for research and publication. Cats

nificance was assumed at ␣ = 0.05.

were anesthetized prior to examination (Williams et al., 2002) in

accordance with the clinic’s protocols.

Cats were aged by dentition (Humane Society of the United 3. Results

States (HSUS), 1996) and grouped into 3 categories: less than 6

months of age (<6mo), between 6 months and 2 years of age 3.1. Feline population

(6mo–2yr), and greater than 2 years of age (>2yr) at time of pre-

sentation (Holmstrom et al., 2013; Vogt et al., 2010). Additional A total of 941 cats were presented during eight clinics held

information collected included the physical location from which January–May and September–November 2014. Cats were trapped

they were trapped and coat length (Dallas et al., 2006). throughout the state of Oklahoma and from southern Kansas. Of

Sampling corresponded with the dates of the trap-neuter- these, 673 cats (71.5% of all cats presented to the TNR clinic) were

return clinic, occurring once each month from January–May and examined for flea and tick infestation (Table 1). Ages were recorded

September–November 2014. for 658 of the cats studied for fleas and ticks: 142 cats (21.6%) were

<6mo, 385 (58.5%) were 6mo–2yr, and 131 (19.9%) were >2yr.

Hair samples from 589 cats (62.6% of all cats presented to the

2.2. Fleas and ticks

TNR clinic) were analyzed for lice and fur mites from March–May

and September–November. Ages were recorded for 520 of the cats

Cats were examined for fleas and ticks by parting the coat and

from which hair samples were collected; 80 (15.4%) were <6mo,

visually examining for ectoparasites, as well as combing through

325 (62.5%) were 6mo–2yr, and 115 (22.1%) were >2yr.

the coat using a flea comb (Dryden et al., 1994; Marchiondo et al.,

A total of 472 cats (50.2% of all cats presented to the TNR

2013). For the current study, time spent examining a cat and remov-

clinic) were studied for ear mite infestation during the clinics held

ing ectoparasites was limited to 2 min per animal. All ticks found

April–May and September–November. Of the cats examined for

were removed using forceps and recommended removal tech-

ear mite infestation, ages were recorded for 470 animals, and 103

nique (Centers for Disease Control and Prevention (CDC), 2015;

(21.9%) were <6mo, 275 (58.5%) were 6mo–2yr, and 92 (19.6%) were

Marchiondo et al., 2013). Evidence of flea infestation was recorded

>2yr.

when either the presence of fleas or flea frass was noted. Fleas

were caught opportunistically for identification. Flea burden was

3.2. Fleas and ticks

not determined. Fleas and ticks were stored in 100% ethanol until

identification. Fleas were identified using taxonomic keys (Centers

Of 673 cats examined, 479 (71.6%) cats had evidence of flea

for Disease Control and Prevention (CDC), 1969; Fox, 1940; Hopkins

infestation (Table 1). Fleas were found in all months sampled. The

and Rothschild, 1953; Hubbard, 1947; Lewis et al., 1988; Traub

2

prevalence of fleas on cats varied (X = 104.487, df = 7, P = < 0.001)

et al., 1983). Tick species and life stage were identified using tax-

by month. The prevalence of fleas or flea dirt was highest in January,

onomic keys (Clifford et al., 1961; Diamant and Strickland, 1965;

September, and October and lowest in April (Supplemental Table 1).

Keirans and Durden, 1998; Keirans and Litwak, 1989).

2

The prevalence of fleas varied (X = 7.948, df = 2, P = 0.019) accord-

ing to the age of cats with infestations detected on 73.3% of cats

2.3. Lice and fur mites

<6mo, 66.0% of cats 6mo–2yr, and 78.5% of cats >2yr. A greater

2

proportion (X = 7.948, df = 1, P = 0.019) of cats >2yr had flea infes-

A 3 cm × 3 cm section of fur was clipped over the jugular furrow

tations in comparison to cats 6mo–2yr.

from the ventral portion of the animal’s neck to facilitate venipunc-

Identifications were determined for 1117 fleas collected from

ture. This hair was collected and placed in an individual, sealed

322 cats. Between 1 and 25 fleas were collected per cat. Cteno-

plastic bag in 70% isopropanol until examination. Fur samples were

cephalides felis was identified on 313 (97.2%) cats, Pulex spp. on 9

analyzed for 3 min each under dissecting microscope for presence

(2.8%) cats, Cediopsylla simplex and Nosopsyllus fasciatus were iden-

of lice (Felicola subrostratus) or fur mites (Cheyletiella blakei and

tified on 2 cats each (o.6%, respectively). Two or more fleas were

Lynxacarus radovski). Lice were identified using appropriate refer-

collected from 205 cats. Of these, 199 cats had single species infes-

ences (Bowman, 2014; Zajac and Conboy, 2012).

tation with Ct. felis. One cat had Pulex spp. only. Four cats had dual

J.E. Thomas et al. / Veterinary Parasitology 228 (2016) 17–22 19

Table 1

Number and prevalence of fleas, ticks, and Otodectes cynotis on free-ranging cats in Oklahoma according to month in 2014.

a

Month Parasite No. of cats examined No. of cats infested Prevalence (95% Confidence Interval)

January Fleas 47 41 87.2% (74.6%–94.3%)

3

Ticks 1 2.1% (0.1%–11.3%) Is

O. cynotis NS NS NA

February Fleas 63 29 46.0% (34.1%–58.8%)

3 3

Ticks 2 3.2% (0.5%–10.9%) Aa ; Is

O. cynotis NS NS NA

March Fleas 94 60 63.8% (53.7%–72.9%)

3 2 3

Ticks 14 14.9% (8.9%–23.8%) Aa ; Dv ; Is

O. cynotis NS NS NA

April Fleas 95 41 43.1% (33.4%–53.7%)

2,3 2,3 3 3

Ticks 24 25.3% (17.2%–35.2%) Aa ; Dv ; Is ; Rs

O. cynotis 100 24 24.0% (16.4%–33.4%)

May Fleas 62 41 66.1% (53.2%–76.9%)

2,3 2,3

Ticks 23 37.1% (25.7%–50.0%) Aa ; Dv

O. cynotis 64 7 10.9% (5.3%–20.9%)

September Fleas 122 109 89.3% (82.4%–94.0%)

1,2,3 3

Ticks 29 23.8% (16.7%–32.3%) Aa ; Dv

O. cynotis 119 21 17.6% (11.7%–25.6%)

October Fleas 101 90 89.1% (81.3%–94.2%)

1,2,3 3

Ticks 13 12.9% (7.2%–21.2%) Aa ; Is

O. cynotis 101 22 21.8% (14.8%–31.1%)

November Fleas 89 71 79.8% (70.3%–89.0%)

3

Ticks 20 22.5% (14.7%–32.5%) Is

O. cynotis 86 17 19.8% (12.5%–29.6%)

Total Fleas 673 482 71.6% (68.1%–75.0%)

1,2,3 2,3 3 3

Ticks 126 18.7% (15.9%–21.9%) Aa ; Dv ; Is ; Rs

O. cynotis 470 91 19.4% (15.9%–23.2%)

a 1 2 3

Tick species and life stages found: Aa = Amblyomma americanum; Dv = Dermacentor variabilis, Is = Ixodes scapularis, Rs = Rhipicephalus sanguineus; Larvae, nymph, adult.

infestations of Ct. felis and Pulex spp.; one cat was infested with Cheyletiella blakei was found in 5 of 589 (0.9%; 0.3%–2.0%) hair

both Ct. felis and N. fasciatus. samples. The number of positive samples by month were as follows:

Of 673 cats examined, a total of 373 ticks were found on 126 March (0 of 119), April (0 of 111), May (2 of 62) September (0 of

cats. Ticks were found in all months sampled. The prevalence varied 113), October (1 of 101), and November (2 of 83). In October, one

2

(X = 40.984, df = 7, P = < 0.001) by month (Supplemental Table 1). cat was infested with both F. subrostratus and C. blakei; the cat was

The prevalence of ticks on cats ranged from 2.1% in January to 37.1% also heavily infested with fleas.

in May with an overall prevalence of 18.7% (15.9%–21.9%) (Table 1).

Four tick species were found on the cats: Amblyomma ameri-

3.4. Ear mites

canum, Ixodes scapularis, Dermacentor variabilis, and Rhipicephalus

sanguineus. A. americanum was found on 83 cats, I. scapularis on 41

A total of 472 cats were examined for ear mite infestation dur-

cats, D. variabilis on 13 cats, and R. sanuineus on 1 cat. Two or more

ing the clinics held April–May and September–November 2014.

ticks were collected from 63 cats. Of the cats with multiple ticks

Otodectes cynotis was found in 91 of 472 (19.3%; 15.9%–23.2%) cats

recovered, 36 cats had a single species infestation with A. ameri-

examined. The prevalence of O. cynotis ranged from 10.9% in May

canum, 15 had I. scapularis only, and 1 had D. variabilis only. Six cats

to 23.5% in April (Table 5). A statistically meaningful difference

had a mixed infestation of A. americanum and D. variabilis, while 3 2

(X = 4.899, df = 4, P = 0.298) was not found in the prevalence of O.

were infested with A. americanum and I. scapularis. One cat each had

cynotis infestation according to the month cats were sampled nor

the following dual infestations: A. americanum and R. sanguineus; I. age.

scapularis and D. variabilis. One cat was infested with three species

of ticks: A. americanum, I. scapularis, and D. variabilis. All motile life

4. Discussion

stages of ticks were found including larvae, nymphs, and adults of

A. americanum; nymphs and adults of D. variabilis, adult I. scapu-

While management of free-roaming cats is a controversial topic

laris, and adult R. sanguineus (Tables 1 and 2). The burden of ticks

(American Veterinary Medical Association (AVMA), 2016; Ash and

on cats ranged from 1 to 40 ticks per cat. These cats with more than

Adams, 2003; Wald and Jacobson, 2014), these animals provide an

10 ticks per cat comprised 32.2% of the ticks recovered. The major-

invaluable resource for studying ectoparasite burdens. Community

ity of these ticks were A. americanum (92.5%) comprised of adults

cats share the same outdoor environment with cats, but tradi-

(12.6%), nymphs (32.4%), and larvae (55.0%). The remainder were

tionally do not receive routine veterinary care including insecticide

adults and nymphs of D. variabilis and I. scapularis. The cat with 40

or acaricide application. This allows for evaluation of ectoparasite

ticks was infested with 5 nymphs and 35 larvae of A. americanum.

risk for both owned and non-owned animals.

Fleas commonly infest domestic cats (Dryden et al., 1994), and

3.3. Lice and fur mites 71.6% cats examined in the current study had evidence of flea infes-

tation. This is consistent with a shelter survey conducted in the

A total of 589 hair samples were analyzed from March–May and same region as the current study, which showed evidence of flea

September–November 2014. Felicola subrostratus was found in 6 infestation on 73.3% (85 of 116) of cats (Little et al., 2015). Fleas were

of 589 (1.0%; 0.5%–2.2%) of hair samples. The number of positive found in all months studied and the prevalence of flea infestation

samples by month were as follows: March (1 of 119), April (0 of ranged from 43.1% in April to 89.3% in September.

111), May (1 of 62), September (3 of 113), October (1 of 101), and In a similarly conducted ectoparasite study of free-roaming cats

November (0 of 83). presented to a TNR program in Florida, 92.5% of the animals were

20 J.E. Thomas et al. / Veterinary Parasitology 228 (2016) 17–22

Table 2

Species and life stages of ticks recovered from free-ranging cats in Oklahoma.

Species Adult Nymph Larva Total

Amblyomma americanum 69 (46 females, 23 males) 103 94 266

Ixodes scapularis 84 (63 females, 21 males) 0 0 84

Dermacentor variabilis 12 (8 females, 4 males) 7 0 19

Rhipicephalus sanguineus 4 (1 female, 3 males) 0 0 4

Total 169 (118 females, 51 males) 110 94 373

found to be infested with fleas, but prevalence was not found to cats, with immature, motile stages comprising 54.7% of all ticks

vary by month (Akucewich et al., 2002). Climate and time of year found. Our results were consistent with other studies, in which lar-

likely account for the differences in flea prevalence between these val and nymphal ticks accounted for up to 61.1% of ticks infesting

studies. Despite high flea prevalences reported in ectoparasite stud- domestic cats (Bishopp and Trembley, 1945; Burroughs et al., 2016;

ies, they are likely overlooked during routine physical examination Magnarelli et al., 1990).

at veterinary hospitals. In a nationwide study, flea infestation was Though at least nine species of ticks have been reported to infest

a reported finding on only 9.2% of cats during examination (Lund domestic cats in the United States (Bishopp and Trembley, 1945),

et al., 1999). The high prevalence of fleas on free-roaming domestic both immature and mature stages of four tick species were found

cats suggest that risk to owned domestic cats is high and substan- in the current study: A. americanum, D. variabilis, I. scapularis, and

tiates year-round used of labeled flea preventives. R. sanguineus. Additional tick species and life stages may have been

In the current study, four flea species were found infesting detected if the TNR clinic was conducted each month of the year

domestic cats: Ct. felis, Pulex spp., C. simplex and N. fasciatus. All when other tick species are more active.

four species of fleas found in the current study have been reported It was somewhat surprising to find R. sanguineus on only 1 cat in

on wildlife in the surrounding regions (Eddy, 1943; Ellis, 1955; the current study. Though consistent with other reports from the

Portman, 1944). The wildlife-associated flea species, C. simplex United States (Akucewich et al., 2002; Burroughs et al., 2016), these

and N. fasciatus, could have resulted from exposure while pre- results are dissimilar to other studies (Mendes-de-Almeida et al.,

dating wildlife or could be reflective of habitat and lifestyle of 2011) which found that 1.4% of all cats examined were infested

free-roaming cats. with R. sanguineus. Worldwide, over ten Rhipicephalus spp. have

In contrast to fleas, there are few primary literature reports of been documented to infest domestic cats (Walker et al., 2000).

ticks naturally infesting cats in the United States (Adolph, 2013; R. sanguineus is known to infest premises, and the free-roaming

Akucewich et al., 2002; Anderson and Magnarelli, 1980; Bishopp nature of the current study’s cat population may account for the

and Trembley, 1945; Burroughs et al., 2016; Curran and Fish, 1989; decreased prevalence in comparison to urban or owned popula-

Magnarelli et al., 1990). This may stem from the common mis- tions. Additionally, Rhipicephalus spp. have shortened mouthparts,

perception that cats are not suitable hosts for ticks, are fastidious which may allow cats to more successfully remove them by groom-

groomers, or from difficulty in conducting such studies. Of ticks ing. This is unlikely the sole reason for a low observed prevalence,

recovered in veterinary clinics, less than 2% are recovered from cats as another tick with shortened mouthparts, D. variabilis, accounted

in comparison to dogs (Burroughs et al., 2016), which may lead vet- for 5.1% of ticks collected in this study. The R. sanguineus group is

erinary professionals to underestimate this ectoparasite burden. currently undergoing re-classification (Dantas-Torres et al., 2013).

However, cats are brought to a veterinarian with decreased fre- As more is learned about genetic and behavioral differences, it may

quency in comparison to dogs (Volk et al., 2011) and usually are less be determined that one or more R. sanguineus species are present in

than willing participants in a thorough examination. Challenges the United States. The Rhipicephalus species present in the United

encountered during laboratory infestations appear to perpetuate States may be less accepting of a felid host.

the belief that only certain tick species and life stages will feed on Felicola subrostratus, was found on roughly 1% of cats sam-

cats (Marchiondo et al., 2013). The common occurrence of ticks on pled in the current study. Though this prevalence is in agreement

free-roaming domestic cats suggest that risk to owned domestic with a similar study conducted on feral cats in Florida (Akucewich

cats is high and warrants year-round used of labeled acaricides. et al., 2002), it may underrepresent natural infestation due to site

To the authors’ knowledge, the current study comprises the predilection on the host. F. subrostratus is most commonly iden-

most ticks reported from naturally infested domestic cats in the tified on the head and dorsum of the animal (Wall and Shearer,

United States to date. The 373 ticks identified account for greater 2001) but may occur almost anywhere (Bowman, 2014; Mullen

than 70% of all primary reports of ticks naturally infesting U.S. and Durden, 2002). The walking dandruff mite, Cheyletiella blakei,

domestic cats. Over eighteen percent (18.7%) of cats examined were was found on 0.85% of cats sampled, an increased prevalence com-

infested with ticks, with a prevalence as high as 37.1% during one pared to other studies (Akucewich et al., 2002). The area of hair

month of the study. It’s likely that even the current study under- collection in the current study was closer to C. blakei’s natural site

estimated tick prevalence and burden due to the time limitation of predilection of the cat’s head and dorsal surface (Bowman, 2014;

2 min to examine each animal, as well as the difficulty in finding and Wall and Shearer, 2001). Lynxacarus radovskyi is considered rare

recovering immature ticks within a short duration. Our results were in (Zajac and Conboy, 2012) and was not observed

consistent with the work of Magnarelli et al. (1990) in the north- on any cats in the current study. When found, L. radovskyi tends to

eastern United States, which showed 23.7% of owned, domestic be located on the cat’s dorsal surface, at terminal parts of the hair

cats examined were infested with ticks. Tick-borne disease stud- (Bowman, 2014; Miller et al., 2013).

ies have reported up to 15.5% (25 of 161) of healthy domestic cats Otodectes cynotis was detected in 19.3% of cats examined in the

presented to veterinary clinics are PCR-positive for Cytauxzoon felis current study. In United States veterinary hospitals, ear mites were

in enzootic areas (Rizzi et al., 2015), suggesting that tick infestation only recognized in 7.4% of feline patients during examination (Lund

is not unique to free-roaming cats. et al., 1999). Increased prevalence in feral cats may be explained

Infestation of domestic cats by immature tick life stages (lar- by the differences in habitat between the two populations, or

vae, nymphs) is underappreciated. In the current study, all motile may signal that O. cynotis goes undetected in some veterinary

life stages of ticks (larvae, nymphs, and adults) were present on patients. Between 11–15% of cats with normal-appearing ears may

J.E. Thomas et al. / Veterinary Parasitology 228 (2016) 17–22 21

be infested with O. cynotis (Akucewich et al., 2002; Sotiraki et al., Anderson, J.F., Magnarelli, L.A., 1980. Vertebrate host relationships and distribution

of ixodid ticks (: Ixodidae) in Connecticut, USA. J. Med. Entomol. 17,

2001), necessitating the need for proper diagnosis and routine

314–323.

treatment with effective parasiticides.

Ash, S.J., Adams, C.E., 2003. Public preferences for free-ranging domestic cat (Felis

catus) management options. Wildl. Soc. B 31 (2), 334–339.

Bishopp, F.C., Trembley, H.L., 1945. Distribution and hosts of certain North

5. Conclusions

American ticks. J. Parasitol. 31, 1–54.

Bowman, D.D., 2014. Georgis’ Parasitology for Veterinarians, 10th edition. Elsevier

Health Sciences, Saunders St. Louis, Missouri, USA, 477 pp.

Cats were found naturally infested with fleas, ticks, lice, fur

Burroughs, J.E., Thomasson, J.A., Marsella, R., Greiner, E.C., Allan, S.A., 2016. Ticks

mites, and ear mites. Ectoparasites were found in all months sam-

associated with domestic dogs and cats in Florida, USA. Exp. Appl. Acarol. 69,

pled, validating current recommendations for year-round use of 87–95.

approved ectoparasiticides. This study highlights the prevalence of Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., et al., 1997. Parasitology meets

ecology on its own terms: margolis revisited. J. Parasitol., 575–583.

natural tick infestations on cats. In fact, the ticks reported in the

Centers for Disease Control and Prevention (CDC), 1969. Pictorial keys to

current study account for over 70% of all primary reports of natu-

, reptiles, birds and mammals of public health significance. Centers

ral tick infestations on cats in the United States to date. Ticks were for Disease Control and Prevention (CDC), United States Department of Health

and Human Services Atlanta, GA, 192 pp.

found in all months studied, and immature, motile stages of ticks

Centers for Disease Control and Prevention (CDC), 2015. Tick removal and testing.

(larvae, nymphs) are an underappreciated source of tick burden on

National Center for Emerging and Zoonotic Infectious Diseases, Division of

domestic cats. Vector-Borne Diseases. Page last updated: November 5, 2015. Last accessed:

April 4, 2016. .

Clifford, C.M., Anastos, G., Elbl, A., 1961. The larval ixodid ticks of the eastern

Conflict of interest statement United States (Acarina-Ixodidae). Miscellaneous publications of the

entomological society of america. Entomol. Soc. Am. 2, 215–237.

Curran, K.L., Fish, D., 1989. Increased risk of Lyme disease for cat owners. N. Engl. J.

In the past five years, MVR and JET have received honoraria and

Med. 320, 183.

research support from multiple veterinary pharmaceutical compa- Dallas, S., North, D., Angus, J., 2006. Grooming Manual for the Dog and Cat.

Blackwell Publishing, Ltd., Ames, Iowa, USA, 258 p.

nies. These activities were unrelated to the current study.

Dantas-Torres, F., Latrofa, M.S., Annoscia, G., Parisi, A., Otranto, D., 2013.

Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato

Funding from the New and Old Worlds. Parasit. Vectors 6, 213.

Diamant, G., Strickland, R.K., 1965. Manual on Livestock Ticks for Animal Disease

Eradication Division Personnel. Publication ARS 91–49, United States

Thank you to William and Esther Barrow and Melanie Beardon-

Department of Agriculture, Agricultural Research Service, USA, 142 pp.

Foster for donation of consumable supplies for sample collection. Dryden, M.W., Boyer, J.E., Smith, V., 1994. Techniques for estimating on-animal

populations of Ctenocephalides felis (Siphonaptera: Pulicidae). J. Med. Entomol.

This research did not receive any specific grant from funding agen-

31, 631–634.

cies in the public, commercial, or not-for-profit sectors.

Eddy, G.W., 1943. Some fleas collected from the Oklahoma cottontail rabbit,

Sylvilagus floridanus alacer (Bangs). J. Kansas Entomol. Soc. 16, 1–3.

Ellis Jr., L.L., 1955. A survey of the ectoparasites of certain mammals in Oklahoma.

Responsibilities

Ecology 36, 12–18.

Fox, I., 1940. Fleas of Eastern United States. The Iowa State College Collegiate Press,

Ames, Iowa, USA, 191 pp.

JET and MVR were responsible for study design, IACUC approval,

Holmstrom, S.E., Bellows, J., Juriga, S., Knutson, K., Niemiec, B.A., Perrone, J., 2013.

primary parasite collection, taxonomic keying, statistical analyses,

AAHA dental care guidelines for dogs and cats. J. Am. Anim. Hosp. Assoc. 49,

and drafting of the manuscript. LS assisted with logistics and criti- 75–82.

cal manuscript revisions. JG assisted in parasite collection, sample Hopkins, G.H.E., Rothschild, M., 1953. An Illustrated Catalogue of the Rothschild

Collection of Fleas (Siphonaptera) in the British Museum (Natural History)

analysis, and data curation. All authors have approved the final

with Keys and Short Descriptions for the Identification of Families, Genera,

version of this manuscript for publication.

Species and Subspecies. Tungidae and Pulicidae, vol. I. The University Press,

Cambridge, UK, 361 pp.

Hubbard, C.A., 1947. Fleas of Western North America. In: Their Relation to the

Acknowledgements

Public Health. The Iowa State College Press, Ames, Iowa, USA, 533 pp.

Humane Society of the United States (HSUS), 1996. How to determine a cat’s or

dog’s age. Animal Sheltering 19, suppl.

The authors thank Zaria Vick, Carlye Hiebert, Yoko Nagamori,

Keirans, J.E., Durden, L.A., 1998. Illustrated key to nymphs of the tick

and Jeff Gruntmeir for assistance with data and sample collection

Amblyomma (Acari: Ixodidae) found in the United States. J. Med. Entomol. 35,

during the Operation Catnip events. The authors also thank Megan 489–495.

Keirans, J.E., Litwak, T.R., 1989. Pictorial key to the adults of hard ticks,

Dayton and Chelsey Lufkin for helping coordinate Operation Catnip

Ixodidae (Ixodida: Ixodoidea), east of the Mississippi River. J. Med. Entomol.

Stillwater and all of the student and community volunteers that

26, 435–448.

make the program a success. Lewis, R.E., Lewis, J.H., Maser, C., 1988. The Fleas of the Pacific Northwest. Oregon

State University Press Corvallis, Oregon, USA, 296 pp.

Little, S., Adolph, C., Downie, K., Snider, T., Reichard, M., 2015. High prevalence of

Appendix A. Supplementary data covert infection with gastrointestinal helminths in cats. J. Am. Anim. Hosp.

Assoc. 51, 359–364.

Lund, E.M., Armstrong, P.J., Kirk, C.A., Kolar, L.M., Klausnor, J., 1999. Health status

Supplementary data associated with this article can be found,

and population characteristics of dogs and cats examined at private veterinary

in the online version, at http://dx.doi.org/10.1016/j.vetpar.2016.07.

practices in the United States. J. Am. Vet. Med. Assoc. 214, 1336–1341.

034. Magnarelli, L., Anderson, J., Levine, H., Levy, S., 1990. Tick and

antibodies to Borrelia burgdorferi in cats. J. Am. Vet. Med. Assoc. 197, 63–66.

Marchiondo, A.A., Holdsworth, P.A., Fourie, L.J., Rugg, D., Hellman and, K., Snyder,

References D.E., 2013. World Association for the Advancement of Veterinary Parasitology

(W.A.A.V.P.) second edition: guidelines for evaluating the efficacy of

parasiticides for the treatment, prevention and control of flea and tick

Adolph, C.B., 2013. Prevalence, Disease Implications, and Diagnostic Assays for

infestations on dogs and cats. Vet. Parasitol. 194, 84–97.

Parasites and Vector-borne Infections of Cats in Northeastern Oklahoma.

Mendes-de-Almeida, F., Crissiuma, A.L., Gershony, L.C., Willi, L.M.V., Paiva, J.P.,

Master of Science Center for Veterinary Health Sciences, Oklahoma State

Guerrero, J., Labarthe, N., 2011. Characterization of ectoparasites in an urban

University, Stillwater, Oklahoma, USA, 94 pp.

cat (Felis catus Linnaeus, 1758) population of Rio de Janeiro, Brazil. Parasitol.

Akucewich, L.H., Philman, K., Clark, A., Gillespie, J., Kunkle, G., Nicklin, C.F., Greiner,

Res. 108, 1431–1435.

E.C., 2002. Prevalence of ectoparasites in a population of feral cats from north

Miller, W.H., Griffin, C.E., Campbell, K.L., Muller, G.H., 2013. Muller and Kirk’s Small

central Florida during the summer. Vet. Parasitol. 109, 129–139.

Animal Dermatology, 7th edition. Elsevier Health Sciences, St. Louis, Missouri,

American Veterinary Medical Association (AVMA), 2016. Free-roaming Abandoned

USA, pp. 284–362.

and Feral Cats. AVMA Policy, January 9, 2016 revision. Last accessed: April 4,

Mullen, G., Durden, L.A., 2002. Medical and Veterinary Entomology, 1st edition.

2016.

and-Feral-Cats.aspx/>. Academic Press San Diego, CA, USA, 597 pp.

22 J.E. Thomas et al. / Veterinary Parasitology 228 (2016) 17–22

Portman, R.W., 1944. Winter distribution of two ectoparasites of the cottontail Vogt, A.H., Rodan, I., Brown, M., Brown, S., Buffington, C.T., Forman, M.L., Neilson, J.,

rabbit in Missouri. J. Econ. Entomol. 37, 541. Sparkes, A., 2010. AAFP-AAHA feline life stage guidelines. J. Feline Med. Surg.

Rózsa, L., Reiczigel, J., Majoros, G., 2000. Quantifying parasites in samples of hosts. 12, 43–54.

J. Parasitol. 86, 228–232. Volk, J.O., Felsted, K.E., Thomas, J.G., Siren, C.W., 2011. Executive summary of the

Reiczigel, J., 2003. Confidence intervals for the binomial parameter: some new Bayer veterinary care usage study. J. Am. Vet. Med. Assoc. 238, 1275–1282.

considerations. Stat. Med. 22, 611–621. Wald, D.M., Jacobson, S.K., 2014. A multivariate model of stakeholder preference

Rizzi, T.E., Reichard, M.V., Cohn, L.A., Birkenheuer, A.J., Taylor, J.D., Meinkoth, J.H., for lethal cat management. PLoS One 9, e93118.

2015. Prevalence of Cytauxzoon felis infection in healthy cats from enzootic Walker, J.B., Keirans, J.E., Horak, I.G., 2000. The Genus Rhipicephalus (Acari,

areas in Arkansas, Missouri, and Oklahoma. Parasit.Vectors 8, 1–6. Ixodidae): a Guide to the Brown Ticks of the World. Cambridge University

Shock, B.C., Moncayo, A., Cohen, S., Mitchell, E.A., Williamson, P.C., Lopez, G., Press, Cambridge, UK, 643 pp.

Garrison, L.E., Yabsley, M.J., 2014. Diversity of piroplasms detected in blood-fed Wall, R., Shearer, D., 2001. Veterinary Ectoparasites: Biology, Pathology and

and questing ticks from several states in the United States. Ticks Tick Borne Control, 2nd edition. Wiley-Blackwell Malden, MA, USA, 304 pp.

Dis. 5, 373–380. Williams, L.S., Levy, J.K., Robertson, S.A., Cistola, A.M., Centonze, L.A., 2002. Use of

Sokal, R., Rohlf, F., 1997. Biometry, 3rd edition. W.H Freeman and Company New the anesthetic combination of tiletamine, zolazepam, , and xylazine

York, NY, USA, 880 pp. for feral cats. J. Am. Vet. Med. Assoc. 220, 1491–1495.

Sotiraki, S., Koutinas, A., Leontides, L., Adamama-Moraitou, K., Himonas, C., 2001. Zajac, A.M., Conboy, G.A., 2012. Veterinary Clinical Parasitology, 7th edition.

Factors affecting the frequency of ear canal and face infestation by Otodectes Blackwell Publishing Ames, IA, USA, 305 pp.

cynotis in the cat. Vet. Parasitol. 96, 309–315.

Traub, R., Rothschild, M., Haddow, J.F., 1983. The Rothschild Collection of Fleas. The

Ceratophyllidae: Key to the Genera and Host Relationships. With Notes on

Their Evolution, Zoogeography, and Medical Importance. Published privately

by Miriam Rothschild & Robert Traub, Cambridge, UK, 288 pp.