AN ASSESSMENT OF THE CLINICAL EFFICACY OF PYRANTEL PAMOATE AS THE ANTEHELMINTH TREATMENT OF CHOICE

IN AN OPEN ADMISSION SHELTER IN PASCO COUNTY, FLORIDA.

By JALEH KHORSANDIAN-FALLAH, DVM

SPECIAL PROJECT

DEPARTMENT OF GLOBAL HEALTH COLLEGE OF PUBLIC HEALTH

UNIVERSITY OF SOUTH FLORIDA TAMPA, FLORIDA

JULY 2015

APPROVED:

___________________________________ _____ Project Supervisor Name & Degrees Date

___________________________________ ______ Second Reader Name & Degrees Date

�

i"

TABLE OF CONTENTS

List of Tables ........................................................................................................... iii List of Figures .......................................................................................................... iv Abstract .................................................................................................................... v. Chapter One: Introduction ........................................................................................ 1 Background ..................................................................................................... 1 Setting ............................................................................................................. 6 Purpose ........................................................................................................... 7 Chapter Two: Methods ............................................................................................. 8 Collection ........................................................................................................ 8 Processing ....................................................................................................... 8 Chapter Three: Results ............................................................................................ 10 Chapter Four: Discussion ........................................................................................ 12 Chapter Five: Recommendations ............................................................................ 15 Deworming Protocols ................................................................................... 15 Intake Recommendations ............................................................................. 16 Monthly Recommendations .......................................................................... 17 Adoption Recommendations ........................................................................ 18 Screening Recommendations ....................................................................... 19 Environmental Control Recommendations .................................................. 19 Client and Staff Education Recommendations ............................................. 20 Recommendations for Further Study ............................................................ 21 Strengths of Study ........................................................................................ 21 Limitations of Study ..................................................................................... 21

ii"

Chapter Six: Conclusions ........................................................................................ 23 References ............................................................................................................... 24

!iii!

LIST OF TABLES

Table 1: Drug Cost Comparison Chart ........................................................ 15 Table 2: Drug Comparison Chart ..................................................................... 16

!iv!

LIST OF FIGURES

Figure 1: Pasco County Vector Map .................................................................. 10

!v!

Abstract

With the emergence of highly effective monthly anti-parasitic treatments in the United

States, the prevalence of intestinal parasites has fallen dramatically in the owned pet population

(Gates & Nolan, 2014)(Irwin, 2002). However, the stray animal population remains an untreated

group with high rates of exposure to parasitic organisms. Intestinal parasitism is common in

animal shelters; with roundworm, whipworm, and hookworms prevalent (Blaburn BL, Lindsay

DS, Vaughn JL, 1996) (Little et al., 2009)(Anna Ortuñoa, 2014). These parasites are classified as

zoonotic agents, although human infections are uncommon in the United States and are generally

associated with the young, elderly, and immunocompromised (I D Robertson, Irwin, Lymbery, &

Thompson, 2000). Treatment of intestinal parasites is necessary to ensure individual and herd

health, prevent environmental contamination, and limit exposure of the general public (Traversa

et al., 2014). Due to limitations in shelter resources, individual fecal screening at time of shelter

admission is not feasible (Giulia Simonato, Antonio Frangipane di Regalbono, Rudi Cassini,

Donato Traversa, Paola Beraldo, Cinzia Tessarin, 2015)(Little et al., 2009). The high presence of

parasitic infections in shelter animals(Blaburn BL, Lindsay DS, Vaughn JL, 1996) (Anna

Ortuñoa, 2014) is such that prophylactic anthelminthic treatment is considered a standard of care

for most public shelters. Effective treatment protocols for intestinal helminthes in the shelter

setting should be based on parasitic prevalence, ease of administration, and cost effectiveness.

The purpose of this study is to assess the efficacy of single dose pyrantel pamoate at 10mg/kg as

the sole anthelmintic agent in shelter dogs after admission to Pasco County Animal Services

!vi!

(PCAS). 58 of 67 sampled animals screened positive for intestinal parasites, indicating an 86.5%

intestinal parasite disease prevalence of the intake dog population. Pyrantel pamoate was found

clear 100% of all roundworm infections, 12.1% of all hookworm infections, and 0% clearance of

whipworms. Based on prevalence data and clinical efficacy findings, pyrantel pamoate at

10mg/kg as the sole anthelminthic agent at PCAS is ineffective intervention. Alternate

deworming protocols should be pursued based on spectrum effects, ease of compliance, and cost

considerations.

!1

CHAPTER 1

INTRODUCTION

Background

The presence of intestinal parasites in our companion animals is of human public health

importance, due to the intimate association of humans and animals (Zasloff & Kidd,

1994)(Waltner-Toews, 1993). Companion animals live in extremely close association with

people, often eating, defecating, sleeping and performing grooming behaviors within the

confines of the home and surrounding green areas (Robertson, Irwin, Lymbery, & Thompson,

2000)(Paoletti et al., 2015). The control of parasites in companion animals is necessary to limit

the exposure of humans to zoonotic disease. Zoonotic infections transmitted from the domestic

canine are varied and include but are not limited to the following: cutaneous larva migrans,

giardiasis, baylisascariasis, microsporidiosis, dipylidiasis, echinococcosis, visceral larva migrans,

ocular larva migrans, neural larva migrans, and trichuriasis (Gavin, Kazacos, & Shulman,

2005)(Georgi & Sprinkle, 1974)(Gavignet, Piarroux, Aubin, Millon, & Humbert,

2008)(Gavignet et al., 2008) (Patricia, Leonor, & Nelson, 2008). Although such infections are

rare, the immunocompromised, elderly, and young are most susceptible to infection. From a

public health perspective, failure to treat carrier animals results in an unnecessary exposure of

the general public (Traversa et al., 2014)(Sandhu & Singh).

Control of parasites in the domestic dog has additional public health consequences in the

instance of publicly funded public health agencies, such as animal services. The control and care

!2

of stray animals in our community is often an unappreciated public health service in the United

States. One has only to look to less developed nations to see that failure to treat and control the

stray animal population results in increased exposure of humans to zoonotic diseases such as

rabies, larval migrans, infections transmitted by fleas and ticks, and additional intestinal diarrheal

diseases (Mateus, Castro, Ribeiro, & Vieira-Pinto, 2014)(Traub et al., 2014).

Cutaneous larva migrans (also known as creeping eruption) is a human infection of

zoonotic hookworm species. Ancylostoma braziliense and A. caninum are the most common

agents associated with this disease, and are natural pathogens of canines and felines(Bowman,

Montgomery, Zajac, Eberhard, & Kazacos, 2010). The life cycle of Ancyclostoma begins when

eggs are passed in the stool of an infected cat or dog. Within 24 to 48 hours of excretion, the

larvae hatch. The released rhabditiform larvae thrive in moist soil or feces, and after 5 to 10 days

(and two molts) they transform into infective filariform (third-stage) larvae. These infective

larvae remain viable for 3 to 4 weeks under favorable conditions. On contact with the animal

host, the larvae penetrate the epidermis and are transported through the vascular system to the

lungs. The larvae ascend the pulmonary tree until they reach the pharynx, and are swallowed.

The larvae’s final destination is the small intestine, where maturation into sexually mature adults

occurs. Adult worms attach to the intestinal wall with piercing mouthparts and begin to feed and

reproduce. Some larvae become arrested in the tissues, and serve as source of recurrent

infections, known as larval leak. Humans may also become infected when filariform larvae

penetrate the skin. However with most species of hookworm, the larvae cannot mature further in

the human host, and migrate aimlessly within the epidermis. Some larvae may persist in deeper

tissue after finishing their skin migration. Manifestation of hookworm larval migrans may appear

!3

as a pruritic, erythematous creeping eruption. Most forms of infection are self-limiting. (CDC,

2015)(Traub, 2013)(Inpankaew et al., 2014)

Trichuriasis is caused by various species of Trichuris, also known as whipworms. This

family of nematodes does not undergo tissue migration, and larval and adult forms are normally

found only in the intestines. Generally, human cases are caused by Trichuris trichiura, with

zoonotic trichuriasis associated with animal parasites Trichuris vulpis and Trichuris suis.

Trichuris spp. have a direct life cycle, and mature in a single host. Infection of the host occurs

when it ingests embryonated eggs from the environment. The eggs hatch in the small intestine

before finishing their maturation in the large intestine. The adult whipworms are found in the

cecum and adjacent portions of the large intestine, and shed their eggs in the feces. T. vulpis

begins to produce eggs in approximately 70 to 90 days in dogs. Human infections of T. vulpis are

generally silent, but heavy infections may manifest as chronic diarrhea, which may be bloody.

Additional symptoms may include abdominal pain and distention, nausea, vomiting, flatulence,

headache, weight loss, malnutrition, and anemia. Nervousness, anorexia, and urticaria may also

be reported. Untreated and severe infections can lead to clubbing of fingers in children.

Complications from trichuriasis may include rectal prolapse, appendicitis, colitis, and proctitis.

Very rare cases of visceral larva migrans, due to T. vulpis, have been reported in humans (Health,

2005).

Toxocariasis is the parasitic disease caused by the larvae of two species of roundworms:

Toxocara canis and Toxocara cati. The dog is the definitive host of Toxocara canis, with human

acquired infection considered accidental(Gawor, Borecka, Marczyńska, Dobosz, & Żarnowska-

Prymek, 2014). Infected dogs shed unembryonated eggs in their feces, which transform and

become infective in the environment. Following ingestion by the canine host, the eggs hatch and

!4

larvae penetrate the gut wall. The age of the animal determines cycle of the parasite, with

younger dogs undergoing larval migration into the tissues, through the pulmonary tree and into

the gastrointestinal system, until the adult worms develop and oviposit in the small intestine. In

older dogs encystment of larvae into the tissues is more common. Transmammary and

transplacental infection occurs between bitch and pups when encysted stages are reactivated

during late pregnancy. Due to higher rates of shedding, puppies are the major source of

environmental egg contamination. In addition to ingestion of infective eggs, Toxocara canis can

also be transmitted through ingestion of paratenic hosts, via the ingestion of encysted larvae.

Humans are accidental hosts, infected through the ingestion of infective eggs in contaminated

soil, or infected paratenic hosts. After human ingestion, the eggs hatch, larvae penetrate the

intestinal wall and are carried by the circulation to a variety of tissues. (CDC, 2015) While the

larvae do not undergo any further development in these sites, they can cause severe local

reactions that are the basis of toxocariasis. The two main clinical presentations of toxocariasis

are visceral larva migrans and ocular larva migrans, although literature indicates that

toxocadiasis can affect many organs systems. (Carvalho & Rocha, 2011)(Fan, Liao, & Cheng,

2013)(Gavignet et al., 2008)

In the interest of public safety and animal welfare, control of the stray dog population

through rehabilitation and adoption of domesticated dogs is elected over euthanasia of stray

animals in Pasco County. The care of the homeless dog population requires special

consideration, as facilities are generally over crowded with insufficient sanitation practices and

constant influx of infected animals resulting in increased risk of disease transmission of the herd.

With animals coming in from the field daily, the practice of vaccination and deworming of every

animal at intake is vital to the continued health of the individual animals and herd. Failure to

!5

control infectious agents in the animal shelter results in increased morbidity, increased use of

medical resources of each animal, increased length of stay, and decreased adoptability(Litster,

Allen, Mohamed, & He, 2011). All these factors act to drain county resources, increase exposure

of the public to infectious agents, and affect the quality of life for the animals in the shelter.

The current deworming protocol consists of a single does of pyrantel pamoate on

admission, dosed orally at 10mg/kg. Pyrantel pamoate is a combination of pyrantel and pamoic

acid. This agent acts as a depolarizing neuromuscular blocking agent, causing sudden

contraction, followed by paralysis, of the helminthes. In addition, it acts as a cholinesterase

inhibitor and ganglionic stimulant. As a consequence of paralysis, helminthes are unable to

maintain their position in the intestinal lumen and are expelled from the body in the fecal stream

by peristalsis. Pyrantel pamoate is not vermicidal or ovicidal. Not systemically absorbed, this

medication is extremely safe in the young, pregnant, lactating and senior animals. In the dog,

total gut transit time ranges from 1,294 minutes to 3,443 minutes (Boillat, Gaschen, & Hosgood,

2010). This likely translates into an estimated time of oval shedding after deworming of 21.56 to

57.38 hours. Numerous studies have been performed, verifying the efficacy of pyrantel pamoate

against roundworms and hookworms (Kopp, Kotze, McCarthy, Traub, & Coleman, 2008)(Todd,

Crowley, Scholl, & Conway, 1975)(Dryden & Ridley, 1999)(Klein, Bradley, & Conway, 1978).

However, evidence of resistance to pyrantel pamoate has been reported(Kopp, Kotze, McCarthy,

& Coleman, 2007)(Kopp, Coleman, Traub, McCarthy, & Kotze, 2009). It is also of note that

pyrantel pamoate is not effective against whipworms, which is of zoonotic importance (Plumb,

2002).

!6

Setting

Pasco County Animal Services is an open admission shelter, meaning the facility will

accept any animal for any reason. The facility consists of 2 main buildings for the housing and

care of animals. The primary building (Building A) houses the adoption center and support staff,

large and small canine adoptions, feline adoption, feline isolation, feline freedom room,

veterinary services, and several small grass areas for potential adoptions meet and greet.

Building A was constructed with large windows, profuse natural light, and high volume air

turnover air handling systems. The general lighting, air quality, humidity levels, and sound

conduction is fair to good. The large dogs are housed in rectangular runs with coated metal

grates suspended over painted concrete with in-ground outflow drains beneath each run. Cement

block walls separate the lower 4 feet of the runs with chain link fencing extending from the 4 to

8 feet. The large dogs are able to physically interact with adjacent neighbors through the chain

link fence. Small dogs and puppies are housed in small kennels with cement barriers and

stainless steel bar doors. Time spent outside of the kennel is related to walking in a common

grass yard, free run in a common grass enclosure, and smaller communal grass enclosures during

kennel cleaning and adoption meetings.

Building C is the secondary animal housing facility constructed completely of concrete

and retrofitted with an insufficient air handling system. The large dog runs are grouped into 4

sections. Each run is separated from the neighbor with a shared stainless steel barrier extending

from the ground to 4 feet. Chain link extends up from 4 to 8 feet. The animals rest directly on a

painted concrete floor. The in-ground waste drains are positioned directly in front of the run

door. Air quality and lighting is significantly inferior to Building A, with an eye-watering

ammonia smell each morning before cleaning rounds. Time spent out of the runs included

!7

walking on common grass yard, free time in a common grass and dirt play yards, and separate

outdoor grass kennels which were rotated daily between all 4 animal sections.

Cleaning of all animal runs occurs in the morning by animal care technicians and work

release prisoners. Cleaning protocols, deep cleaning protocols, and disinfection protocols are

implemented based on length of animal stay, clinical disease, and movement of animals to

different locations. Fecal waste in the external yards is removed daily and disposed of. Cleaning

and disinfection agents include detergents, trifectant (Potassium peroxymonosulfate 21.41%,

Sodium Chloride 1.5%, Other Ingredients 77.09%), and alternate titrations of bleach. Animal

Care technicians are responsible for determining cleaning protocol (cleaning vs deep clean vs

disinfection) on a daily basis, with veterinarian involvement generally associated with disease

control and training events.

Purpose

The purpose of this study is to evaluate the efficacy of the PCAS’s current deworming

protocol. As the current helminthic prevalence of dogs at PCAS is unknown, a survey will be

conducted to establish baseline data. After prevalence data have been obtained and

geographically mapped within Pasco County, a risk map will be generated. The use of risk maps

and cluster analysis will highlight areas of human exposure to infectious ova produced by the

stray dogs. Establishing prevalence data is also necessary in the creation of an appropriate

deworming protocol.

The second portion of this project is to determine the efficacy of our current deworming

protocol in a clinical shelter setting. The hypothesis tested is that a dog dewormed with a single

dose of pyrantel pamoate at 10mg/kg will test negative for parasite ova in feces 5760- 7200

minutes after deworming event.

!8

CHAPTER 2

METHODS

Collection

Fecal samples were collected from 67 canine animals at intake into PCAS facility during

the month of May 2015, prior to deworming with pyrantel pamoate. Canine intakes include stray

animal, owner surrenders, adoption returns, and animal custody cases. Each animal was assigned

an identification number, and researchers were blinded to an animal’s intake category, location

of origin, previous medical history or fecal flotation results. Fecal samples were collected

directly from animal, or from individual animal housing. A range of 2 to 5 grams of fecal

material is required for analysis by flotation. After collection animals were dewormed as per

standard operating procedure of PCAS. Dosed at 10mg/kg orally, small volumes of pyrantel

pamoate were administered per os. Animals requiring larger volumes of pyrantel pamoate, who

exhibited fractious behavior, or who refused administration of the drug were offered canned diet

with pyrantel pamoate mixed in.

Processing

Fecal flotation was performed on each sample via a zinc sulfate flotation and

centrifugation method. Centrifugation was performed at 1300 rpm for 6 minutes for all samples.

Samples with displaced coverslips during the centrifugation process were floated an additional

10 minutes. All samples were evaluation under 40x microscopy by an experienced veterinary

technician or veterinarian. Animals were followed for 4 to 5 days and a 2nd fecal sample

!9

collected and flotation technique performed. Animals excluded from the study-included animals

treated with additional anthelminthic medications or were released prior to 2nd sample collection.

!10

CHAPTER 3

RESULTS

A total of 67 fecal samples were collected at intake. Of the 67 intake samples collected,

only 9 animals screened “no parasites seen” or NPS. The remaining 58 samples (86.5%)

screened positive for intestinal parasites. In regards to the positive samples; 45 (77.5%) screened

hookworm positive, 13 whipworm positive (22.4%) , 7 roundworm positive (12%), including a

single case of Baylisascaris (1.7%) grouped under roundworms. See figure 1.1

Figure 1 Pasco County Canine Zoonotic Vector Map

!11

A total of 50 samples sets were analyzed to evaluate the efficacy to pyrantel pamoate at

PCAS. Of the 50 intake samples collected, 14 (28%) samples screened NPS. The remaining 36

(72%) samples screened positive for intestinal parasites. In regards to positive samples; 33

(91.6%) screened positive for hookworms, 9 (25%) screened positive for whipworms, 6 (16.7%)

screened positive for round worms, including a single sample of bayliscorsasis. Co-infections

were found in 12 unique animals.

Of the 50 post-deworming samples 19 (38%) samples screened NPS. The remaining 31

(62%) samples screened positive for intestinal parasites. In regards to positive samples; 29

(93.5%) screened positive for hookworms, 10 (32.2%) screened positive for whipworms, 0 (0%)

screened positive for rounds worms, and 1 (3%) sample screened positive for tapeworms. Co-

infections were found in 12 unique animals.

The effectiveness of pyrantel pamoate at 10mg/kg as the sole deworming agent of dogs in

the shelter environment is not sufficiently effective in clearing all ova from stools 4 to 5 days

after deworming. In addition, the single use of pyrantel pamoate at time of intake fails to treat

occult whipworm infections. The failure to eliminate shedding of ova results in a highly

contaminated environment and chronic re-exposure of all kenneled animals, as well as staff,

volunteers, and adopters.

Although pyrantel pamoate displayed 100% clearance of all roundworm infections in this

study, varied levels of hookworm infections persisted. The failure of pyrantel pamoate to

completely eliminate hookworm ova from naturally infected animals appears significant.

!12

CHAPTER 4

DISCUSSION

In cases of most helminth infections, multiple dosing of appropriate anthelmintics are

strongly recommended in conjunction with environmental decontamination and concurrent

treatment of housemates in order to prevent recurrence of parasite infection. The sole use of

pyrantel pamoate for deworming of the canine population at PCAS fails to provide coverage for

prevalent whipworm species, fails to provide coverage for persistent infection via larval leak,

and fails to provide coverage for non-adult stages infection.

Of additional interest is the practical application of pyrantel pamoate in a high volume

shelter setting. The administration of pyrantel pamoate, in conjunction with vaccinations and

topical application of selamectin, occurs at time of admission. Animal control officers or animal

care technicians are generally responsible for application of these interventions. Unfortunately,

intake enrollment is an extremely stressful event for the animals and administration of the oral

medications can be especially challenging, with a high risk of under dosing or failure to medicate

at all. Elaboration of dosing concerns include; failure to appropriately weigh the animal resulting

in under dosages, difficulty administering large volumes of deworming agent, loss of medication

during administration, failure of animal to consume foods where medications are placed, and

failure to medicate fractious or bite quarantine animals. The difficulties of administering

medications are a recurring challenge in the shelter setting, and can significantly affect the

efficacy of our current deworming protocol.

!13

Ideally, an animal shelter-deworming agent would be inexpensive, highly palatable,

single dose, easy to administer, and have an extremely wide margin of safety. Several studies of

multidrug deworming medications have been analyzed in the scientific literature and show high

levels of efficacy against the 4 major intestinal parasites of zoonotic importance (excluding

protozoal organisms) roundworms, hookworms, tapeworms, and whipworms. Multiple studies

have been published, evaluating the efficacy of anthelminthic protocols. Multi drug approach to

anthelminthic treatment is often the most effective. (Lloyd & Gemmell, 1992) produced evidence

for the use of combination praziquantel, pyrantel embonate, and febantel against helminth

infections in dogs with naturally acquired infections. Based on the literature, treatment gave > 97

to 98% reductions in fecal egg counts attributable to Toxascaris leonina, T canis, and Uncinaria

stenocephala with efficacy against Trichuris vulpis at > 92%. Pyrantel pamoate, used in

conjunction with ivermectin as a monthly heartworm preventative gave 100% control of A.

braziliens (Shoop, Michael, Soll, & Clark, 1996) but was not analyzed for control of toxocara

species and is not labeled affective against whipworms or tapeworms. A comparative study

conducted by (Dryden & Ridley, 1999) highlighting pyrantel pamoate and fenbendazole in a

clinical setting showed Greyhounds administered fenbendazole had fecal egg count reductions

(FECRs) of 95.8 and 99.8% at 10 and 31 days following initial treatment, respectively.

Greyhounds administered pyrantel pamoate had FECRs of 85.8 and 88.3% at 10 and 31 days

after the first treatment, respectively. T. canis fecal egg counts conducted from Day 31 through

Day 128 were significant lower in those greyhounds administered fenbendazole as compared to

greyhounds administered pyrantel pamoate. This information highlights the range of efficiency

found in the clinical use of deworming agents. Rinaldi et al. performed a comparative study of

three combination drugs Milbemax® Drontal Plus Flavour® and , Nemex® POP for control of

!14

hookworms, roundworms, whipworms, and tapeworms. At Day -30 intestinal nematodes

(hookworms, Toxocara, Trichuris) and cestodes (Dypilidium caninum) were identified.

Milbemax® , a combination of milbemycin and praziquantel showed 100% efficacy against all

the helminths in all the kennels. Drontal Plus Flavour® , a combination of praziquantel, pyrantel

pamoate and febantel, was 100% effective against hookworms in all the kennels but gave lower

efficacy against T. canis (range#=#97.1-100%) and T. vulpis (range#=#95.6-100%). Nemex® POP,

combination of pyrantel pamoate, oxantel pamoate, and praziquantel was also 100% effective

against hookworms in all kennels but less effective against T. canis (range#=#95.7-100%) and T.

vulpis (range#=#95.7-100%). All three drugs were 100% effective against D. caninum. The use of

Febantel at 15mg/kg administered as a 3.4% paste completely cleared naturally infected dogs of

all nematode and cestode infections, including A. caninum, T. vulpis, Uncinaria stenocephala,

Toxocara canis, Toxascaris leonina, Taenia sp, and Dipylidium caninum. (Corwin, Mccurdy, &

Pratt, 1982).

!15

CHAPTER 5

RECOMMENDATIONS

Deworming Protocols

At this time the intake protocol for dogs at PCAS is based on a single deworming event

with pyrantel pamoate and topical application of selamectin ($9.54). The cost of this intervention

per 50lb dog is approximately $9.75. Based on my experiences at PCAS as staff veterinarian, and

looking at costs involved in treatment as well as dosing regimens I have the following

recommendations based on Table 1 and Table 2

Table 1: Drug Price Comparison Chart for a 50lb dog*

Trade Name Drug Name Dose frequency Cost Milbemycin + Lufenuron Sentinel Monthy $5.84 Milbemycin + Lufenuron + Praziquantel

Sentinel Spectrum Monthly $7.50

Ivermectin + Pyrantel pamoate Trihart Plus Monthly $3.48

Imidacloprid + Moxidectin Advantage

Multi Monthly $11.17 Fenbendazole Panacur 3 days $4.43 Epsiprantel Cestex Once Praziquantelv + Pyrantel + Febantel Drontal plus 1x and repeat $13.88 Febantel Rintal 3 days Pyrantel pamoate Strongid 1x and repeat $0.21 Spinosad + Milbemycin oxime Trifexis Once monthly $11.62 Nitenpyram Capstar as needed $3.18 Fipronil + (S)-methoprene Frontline Plus Monthly $10.81 Imidacloprid + Pyriproxyfen Advantage II Monthly $9.76 Selamectin Revolution Monthly $9.54

!16

*Pricing estimates based on quotes established 7/2015 by MWI Veterinary Supply Accounts

established with PCAS.

Table 1.2 Drug Comparison Chart

Trade Name Drug Name Route

Heart worm

Kills fleas

Round worm

Hook worm

Whip worm

Tape worm

Milbemycin + Lufenuron Sentinel oral + - + + + - Milbemycin + Lufenuron + Praziquantel

Sentinel Spectrum oral + - + + + +

Ivermectin + Pyrantel pamoate

Trihart Plus oral + - + + - -

Imidacloprid + Moxidectin

Advantage Multi topical + + + + + -

Fenbendazole Panacur oral - - + + + Epsiprantel Cestex oral - - - - - + Praziquantelv + Pyrantel + Febantel

Drontal plus oral - - + + + +

Febantel Rintal oral - - + + + - Pyrantel pamoate Strongid oral - - + + - - Spinosad + Milbemycin oxime Trifexis oral + + + + + - Nitenpyram Capstar oral - + - - - Fipronil + (S)-methoprene

Frontline Plus topical - + - - - -

Imidacloprid + Pyriproxyfen

Advantage II topical - + - - - -

Selamectin Revolutio

n topical + + - - - -

Intake Recommendations

• At time of intake animals 8 weeks and older shall be administered Trifexis

($11.62) for control of external and internal parasites.

!17

• In animals where oral dosing is not possible, topical use of Advantage Multi

($11.17) would be a reasonable intervention.

Based on the values of Table 11.2; treating a single 50lb dog at intake would cost

approximately $11.62 - $11.17. At this price point the control of parasites is excellent, with the

administration of a single or tablet given with a meal or a topical agent. Compliance with this

protocol by staff should be high, with a single agent given at time of admission. However,

emesis after administration of Trifexis is not an uncommon adverse reaction, and should factor

into decision making.

• Alternately, Sentinel Spectrum ($7.50) administered at time of intake with a

Capstar ($3.18) would control for external and internal parasites.

• In animals where oral dosing is not possible, topical use of Advantage Multi

($11.17) would be a reasonable intervention.

Based on the values of Table 11.2; treatment of a 50lb dog at time of intake would cost

approximately $10.68- $11.17. At this price point the control of parasites is good, but

compliance may decrease due to administration of two oral drugs.

Monthly Recommendations

Monthly external and internal parasite control should be included as an aspect of the

PCAS deworming protocol. Ideally parasite control should include heartworm prevention, flea

control, and intestinal parasite control.

• Sentinel flavor tabs ($5.84) administered monthly, with the addition of

Capstar ($3.18) as needed would be an ideal kennel treatment.

• Consider the use of Advantage Multi ($11.17) in animals where oral

mediation is not possible.

!18

Cost of monthly treatment per animal would range from $9.02 to $11.17 per 50lb animal.

• A less ideal, and more labor intensive, alternate protocol would involve the

use of ivermectin/pyrantel ($3.48) generic and fenbendazole ($4.43) as well as

a third flea control treatment. At intake all animals would be administered a

single dose of ivermectin/pyrantel generic and capstar ($3.18). Beginning on

day two of intake, medical staff would treat all new animals with 3 days of

fenbendazole.

The estimated cost per 50lb dog at time of intake would be $11.09. The entire herd would

be treated one monthly with ivermectin/pyrantel generic and fenbendazole, and flea control as

needed. Estimate cost of monthly parasite control would range from $7.91 to $11.09. The use of

fenbendazole as the deworming agent, although lower in price per animal, requires more labor of

veterinary services as well as increased risk of noncompliance. This protocol, although initially

more price competitive, is fraught with compliance issues and logistical challenges.

Adoptions Recommendations

• At time of adoptions, clients should be offered a purchase package of 3-month

supply of Sentinel or Trifexis, as well as a single dose of Capstar for control

of infectious parasitic agents.

The use of Sentinel or Trifexis for 3 months will cover for the lifecycle of whipworms

and prevent contamination of the new home environment and housemates with whipworms or

hookworms. The use of Sentinel or Trifexis will also control for any larval leak of hookworms

and roundworms. The single dose of Capstar will effectively kill adult fleas for a 24 to 48 hour

time frame, and break the tapeworm life cycle. By providing a post adoption package, for a

!19

reasonable fee, PCAS will be providing complete coverage for any infectious agents the adopted

animals may have been infected with while homeless or in the shelter environment.

Screening Recommendations

Monitoring of the prevalent helminth species in the shelter population is also a key aspect

of parasite control in the shelter setting. By monitoring our population on a regular basis, we can

note trends in helminth prevalence and well as evaluate the effectiveness of our protocols. The

regular sampling of the population also alerts the veterinary staffing to possible challenges in

compliance, drug efficacy, or possible shifts in parasite burdens in the population as a whole.

Environmental Control Recommendations

With access to so many effective deworming agents in the United States it would seem

that animal shelters should have the herd generally controlled with chemoprophylaxis. However,

animals found roaming and without medical care are often “unthrifty” and suffer from extremely

high worm burdens. In addition, the high rates of ova shedding results in extremely high rates of

parasitic exposure to all animals housed on the facility. Of particular concern as PCAS is the

continued use of dirt runs, grass play areas and grass lawns for dog walks, where

decontamination of sites is not possible. Removal of fecal material in individual and multi-use

areas is inconsistent at best. The subtropical climate of the Pasco Area also creates an idea

humid, moist environment for ova to mature. Desiccation from dry spells or challenges from

freezes do not occur at a level required to curtail parasite transmission. Pasco County’s climate

and location are generally ideal for the helminthes lifecycle. Ideally, dog runs and play areas

would be composed of concrete substrate, which are inhospitable to parasitic ova and larval

forms. Concrete structures may also be cleaned effectively with detergents and water, and be

fully decontaminated in instances of disease outbreaks. Alternate substrates include AstroTurf

!20

and gravel, both of which may be removed from the environment routinely as a part of sanitation

efforts. Removable substrates may also be replaced as needed during disease outbreaks or

quarantine efforts.

Client and Staff Education Recommendations

Controlling helminthic infections in pets is crucial to reduce infection risk for other

companion animals and to minimize public health hazards. Dissemination of understanding and

knowledge of transmission routes, at-risk categories and areas, and control methods are essential

to prevention efforts of humans and animals. Although virtually all of the majority of

roundworms and hookworms affecting dogs and cats may cause human diseases, the public risk

perception in general is poor.

It falls to the PCAS, as a public health agency, in conjunction with veterinarians, to

educate the public about zoonotic disease risk. The percentage of shelter animals examined by

veterinarians after adoption is unknown. However, it is possible to predict compliance based on

the socioeconomic status of the adopters. Educational and awareness interventions, generally at

the time of adoption, may be the only time a person will be exposed to messages regarding

zoonotic disease, basic hygiene, and deworming recommendations. Failure to provide basic

information regarding prevalent zoonotic diseases in shelter animals, especially parasitic

diseases, is a gross failure of the public health systems. Readily available zoonotic disease

pamphlets, verbal client education, and recommendations regarding continuous parasite control

are cost effective means of educating the public and providing the community with basic health

resources.

!21

Recommendations for Future Study

An anonymous staff survey evaluating compliance to current medical protocols as well as

barriers of compliance directed at all levels of staffing would greatly increase our understanding

of the barriers to work compliance found in the stressful shelter environment. A reassessment of

the current medical budget in light of public health concerns with higher levels of administration

including the ACA and additional stakeholders is absolutely necessary for the implementation of

a new deworming protocol. Multiple crossectional studies of parasite prevalence in the housed

population, as well as spot checks of nonclinical adopted animals will further reveal success and

failures in any deworming strategy PCAS implements. In a rapidly changing health environment,

where prevention of infectious diseases is a cornerstone of public health, consistent process

assessment, outcome assessment, and cost-benefit analysis will be necessary to keep the

homeless animals of Pasco County free from zoonotic infections and thereby reduce exposure of

said organisms to the general public.

Strengths of Study

The main strength of this study is in the analysis the efficacy of pyrantel pamoate in the

clinical settings of an animal shelter. This study is not created to argue the literature reviews,

which generally support the use of pyrantel pamoate as a safe and efficacious drug, but to

evaluate this medication in a high stress, high turnover, and highly disease endemic dog

population. This study is highly repeatable, cost effective, and requires no additional training for

veterinarians or veterinary staff.

Limitations Of Study

The current study, while shining a spotlight on ineffective public health practices at

PCAS, fails to address many of the underlying contributing factors. Limitations of this study

!22

include the lack of specification of parasite species based on microscopic analysis, failure to

include ectopic parasites, protozoal organisms and heartworm status of animals in order to

produce a complete profile of parasite burden. In addition, the use of fecal ova reduction counts

instead of binary data would have provided greater insight into the efficacy of the anthelminthic

agents. Statistical analysis of data was not included. The study design also fails to clarify the

cause of outcome. We cannot determine if failure of anthelminthic agent, failure in staff

compliance, or both factors contributes to the study outcome.

!23

Chapter 6

CONCLUSION

In summary, an economical and evidence –based deworming protocol is an essential

component of PCAS’s success as a public health facility. However, the importance of continued

environmental control paired with ongoing staff and volunteer education cannot be ignored.

Finally, providing educational materials to all potential adopters about zoonotic agents found at

PCAS in conjunction with opportunities to continue treatment of prevalent diseases via the

purchase of effective medication will positively impact the health of our human and companion

animal community.

!24

REFERENCES

Boillat, C. S., Gaschen, F. P., & Hosgood, G. L. (2010). Assessment of the relationship between

body weight and gastrointestinal transit times measured by use of a wireless motility

capsule system in dogs. American Journal of Veterinary Research, 71(8), 898–902.

http://doi.org/10.2460/ajvr.71.8.898

Bowman, D. D., Montgomery, S. P., Zajac, A. M., Eberhard, M. L., & Kazacos, K. R. (2010).

Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends in Parasitology,

26(4), 162–7. http://doi.org/10.1016/j.pt.2010.01.005

Carvalho, E. A. A., & Rocha, R. L. (2011). Toxocariasis: visceral larva migrans in children.

Jornal de Pediatria, 87(2), 100–110. http://doi.org/10.2223/JPED.2074

Corwin, R., Mccurdy, H., & Pratt, S. (1982). Effect of febantel against Ancylostome caninum

and Trichuris vulips in dogs. Americal Jounral of Veterinary Research, 43(6), 1100–1102.

Retrieved from

http://apps.webofknowledge.com.ezproxy.lib.usf.edu/full_record.do?product=UA&search_

mode=GeneralSearch&qid=65&SID=2CiE69TpddIISQWbUgD&page=5&doc=41

!25

Dryden, M. W., & Ridley, R. K. (1999). Efficacy of fenbendazole granules and pyrantel pamoate

suspension against Toxocara canis in greyhounds housed in contaminated runs. Veterinary

Parasitology, 82(4), 311–5. Retrieved from

http://www.ncbi.nlm.nih.gov/pubmed/10384907

Fan, C.-K., Liao, C.-W., & Cheng, Y.-C. (2013). Factors affecting disease manifestation of

toxocarosis in humans: genetics and environment. Veterinary Parasitology, 193(4), 342–52.

http://doi.org/10.1016/j.vetpar.2012.12.030

Gavignet, B., Piarroux, R., Aubin, F., Millon, L., & Humbert, P. (2008). Cutaneous

manifestations of human toxocariasis. Journal of the American Academy of Dermatology,

59(6), 1031–42. http://doi.org/10.1016/j.jaad.2008.06.031

Gavin, P. J., Kazacos, K. R., & Shulman, S. T. (2005). Baylisascariasis. Clinical Microbiology

Reviews, 18(4), 703–18. http://doi.org/10.1128/CMR.18.4.703-718.2005

Gawor, J., Borecka, A., Marczyńska, M., Dobosz, S., & Żarnowska-Prymek, H. (2014). Risk of

human toxocarosis in Poland due to Toxocara infection of dogs and cats. Acta

Parasitologica, 60(1), 99–104. http://doi.org/10.1515/ap-2015-0012

Georgi, J. R., & Sprinkle, C. L. (1974). A case of human strongyloidosis apparently contracted

from asymptomatic colony dogs. The American Journal of Tropical Medicine and Hygiene,

23(5), 899–901. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4451229

!26

Health, T. C. for F. S. & P. H. (2005). Trichuriasis. The Center for Food Security & Public

Health. Iowa State University. Retrieved from http:/www.cfsph.iastate.edu/IICAB/

Inpankaew, T., Schär, F., Dalsgaard, A., Khieu, V., Chimnoi, W., Chhoun, C., … Traub, R. J.

(2014). High prevalence of Ancylostoma ceylanicum hookworm infections in humans,

Cambodia, 2012. Emerging Infectious Diseases, 20(6), 976–82.

http://doi.org/10.3201/eid2006.131770

Klein, J. B., Bradley, R. E., & Conway, D. P. (1978). Anthelmintic efficacy of pyrantel pamoate

against the roundworm, Toxocara canis, and the hookworm, ancylostoma caninum, in dogs.

Veterinary Medicine, Small Animal Clinician!: VM, SAC, 73(8), 1011–3. Retrieved from

http://www.ncbi.nlm.nih.gov/pubmed/250990

Kopp, S. R., Coleman, G. T., Traub, R. J., McCarthy, J. S., & Kotze, A. C. (2009). Acetylcholine

receptor subunit genes from Ancylostoma caninum: altered transcription patterns associated

with pyrantel resistance. International Journal for Parasitology, 39(4), 435–41.

http://doi.org/10.1016/j.ijpara.2008.08.005

Kopp, S. R., Kotze, A. C., McCarthy, J. S., & Coleman, G. T. (2007). High-level pyrantel

resistance in the hookworm Ancylostoma caninum. Veterinary Parasitology, 143(3-4), 299–

304. http://doi.org/10.1016/j.vetpar.2006.08.036

Kopp, S. R., Kotze, A. C., McCarthy, J. S., Traub, R. J., & Coleman, G. T. (2008). Pyrantel in

small animal medicine: 30 years on. The Veterinary Journal, 178(2), 177–184.

http://doi.org/10.1016/j.tvjl.2007.06.021

!27

Litster, A., Allen, J., Mohamed, A., & He, S. (2011). Risk factors for delays between intake and

veterinary approval for adoption on medical grounds in shelter puppies and kittens. Preventive

Veterinary Medicine, 101(1-2), 107–112.

Lloyd, S., & Gemmell, M. A. (1992). Efficacy of a drug combination of praziquantel, pyrantel

embonate, and febantel against helminth infections in dogs. American Journal of Veterinary

Research, 53(12), 2272–3. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1476306

Mateus, T. L., Castro, A., Ribeiro, J. N., & Vieira-Pinto, M. (2014). Multiple zoonotic parasites

identified in dog feces collected in Ponte de Lima, Portugal-a potential threat to human

health. International Journal of Environmental Research and Public Health, 11(9), 9050–

67. http://doi.org/10.3390/ijerph110909050

Paoletti, B., Traversa, D., Iorio, R., De Berardinis, A., Bartolini, R., Salini, R., & Di Cesare, A.

(2015). Zoonotic parasites in feces and fur of stray and private dogs from Italy.

Parasitology Research. http://doi.org/10.1007/s00436-015-4402-6

Patricia, N. O., Leonor, J. M., & Nelson, M. S. (2008). Dipylidium caninum infection in a 2 year

old infant: case report and literature review. Revista Chilena de Infectologia, 25(6), 465–

471. Retrieved from

http://apps.webofknowledge.com.ezproxy.lib.usf.edu/full_record.do?product=UA&search_

mode=GeneralSearch&qid=44&SID=2CiE69TpddIISQWbUgD&page=1&doc=5

!28

Plumb, D. C. (2002). Veterinary Drug Handbook (4th ed.). Blackwell Publishing.

Robertson, I. D., Irwin, P. J., Lymbery, A. J., & Thompson, R. C. A. (2000). The role of

companion animals in the emergence of parasitic zoonoses. International Journal for

Parasitology, 30(12-13), 1369–1377. http://doi.org/10.1016/S0020-7519(00)00134-X

Sandhu, G. K., & Singh, D. Level of awareness regarding some zoonotic diseases, among dog

owners of ithaca, new york. Journal of Family Medicine and Primary Care, 3(4), 418–23.

http://doi.org/10.4103/2249-4863.148132

Shoop, W. L., Michael, B. F., Soll, M. D., & Clark, J. N. (1996). Efficacy of an ivermectin and

pyrantel pamoate combination against adult hookworm, Ancylostoma braziliense, in dogs.

Australian Veterinary Journal, 73(3), 84–5. Retrieved from

http://www.ncbi.nlm.nih.gov/pubmed/8660218

Todd, A. C., Crowley, J., Scholl, P., & Conway, D. P. (1975). Critical tests with pyrantel

pamoate against internal parasites in dogs from Wisconsin. Veterinary Medicine, Small

Animal Clinician!: VM, SAC, 70(8), 936–9. Retrieved from

http://www.ncbi.nlm.nih.gov/pubmed/1041522

Traub, R. J. (2013). Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis.

International Journal for Parasitology, 43(12-13), 1009–15.

http://doi.org/10.1016/j.ijpara.2013.07.006

!29

Traub, R. J., Pednekar, R. P., Cuttell, L., Porter, R. B., Abd Megat Rani, P. A., & Gatne, M. L.

(2014). The prevalence and distribution of gastrointestinal parasites of stray and refuge dogs

in four locations in India. Veterinary Parasitology, 205(1-2), 233–8.

http://doi.org/10.1016/j.vetpar.2014.06.037

Traversa, D., Frangipane di Regalbono, A., Di Cesare, A., La Torre, F., Drake, J., & Pietrobelli,

M. (2014). Environmental contamination by canine geohelminths. Parasites & Vectors, 7,

67. http://doi.org/10.1186/1756-3305-7-67

Waltner-Toews, D. (1993). Zoonotic disease concerns in animal-assisted therapy and animal

visitation programs. The Canadian Veterinary Journal. La Revue Vétérinaire Canadienne,

34(9), 549–51. Retrieved from

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1686581&tool=pmcentrez&ren

dertype=abstract

Zasloff, R. L., & Kidd, A. H. (1994). Loneliness and pet ownership among single women.

Psychological Reports, 75(2), 747–52. http://doi.org/10.2466/pr0.1994.75.2.747