Zoonotic Risks from Domestic Animals in Ghana

Abstract

Zoonoses are diseases or infections which are naturally transmitted from vertebrate animals to humans and vice versa. These infections account for more than half of human infections worldwide, with most cases reported in developing countries like Ghana. The Government of Ghana recently launched the “Rearing for Food and Jobs Campaign”, an initiative to bridge the glaring deficit in protein supply. This has resulted in increased livestock production nationwide in response to the increasing demand for animal protein. Increase in both human and livestock population in the country have implications for transmission of zoonotic diseases, as it allows for more frequent interactions between the two within a limited space. Multiple animals are kept in various homes at varying levels of confinement. Security concerns, particularly in urban areas, have resulted in an increased reliance on dogs, while financial considerations have mainly driven a rapid increase in livestock production both at commercial and smallholder levels. Taking into account that the pandemics in the past few decades have animal origins, this growing human-animal interconnection is of concern. Albeit an increased household-human-animal ratio, there is a paucity of epidemiological data on domestic animals in Ghana. Several zoonotic diseases have been reported in Ghana, including rabies, toxocariasis, toxoplasmosis, Q-fever, hepatitis E and brucellosis. Risk factors such as close contact with animals, poor hand hygiene, poor sanitation, and unvaccinated, free-ranging animals have been linked with zoonotic transmissions. Zoonoses have been recorded in homes, slaughterhouses, and on farms in farm workers, butchers, and vulnerable groups, including children, pregnant women, and HIV patients. A ‘One-Health’ approach, which comprises well-coordinated activities of both health and veterinary services, will facilitate timely diagnosis and effective control of zoonoses in Ghana.

Full text

_____________________________________________________________________________________________________
*Corresponding author: Email: kofireynolds@gmail.com;
International Journal of Pathogen Research
4(3): 17-31, 2020; Article no.IJPR.57959
ISSN: 2582-3876
Zoonotic Risks from Domestic Animals in Ghana
Papa Kofi Amissah-Reynolds
1*
1
Department of Science Education, Faculty of Science and Environment Education,
College of Agriculture Education, Asante-Mampong, University of Education, Winneba, Ghana.
Author’s contribution
The sole author designed, analyzed and interpreted and prepared the manuscript.
Article Information
DOI: 10.9734/IJPR/2020/v4i330113
Editor(s):
(1)
Dr. Mayada Mosad Ahmed Gwida, Mansoura University, Egypt.
Reviewers:
(1) Ehsan Gharib Mombeni, Shahid Chamran University of Ahwaz, Iran.
(2)
Abu Hasan Sarkar, India.
Complete Peer review History:
http://www.sdiarticle4.com/review-history/57959
Received 02 April 2020
Accepted 08 June 2020
Published 20 June 2020
ABSTRACT
Zoonoses are diseases or infections which are naturally transmitted from vertebrate animals to
humans and vice versa. These infections account for more than half of human infections
worldwide, with most cases reported in developing countries like Ghana. The Government of
Ghana recently launched the “Rearing for Food and Jobs Campaign”, an initiative to bridge the
glaring deficit in protein supply. This has resulted in increased livestock production nationwide in
response to the increasing demand for animal protein. Increase in both human and livestock
population in the country have implications for transmission of zoonotic diseases, as it allows for
more frequent interactions between the two within a limited space. Multiple animals are kept in
various homes at varying levels of confinement. Security concerns, particularly in urban areas,
have resulted in an increased reliance on dogs, while financial considerations have mainly driven a
rapid increase in livestock production both at commercial and smallholder levels. Taking into
account that the pandemics in the past few decades have animal origins, this growing human-
animal interconnection is of concern. Albeit an increased household-human-animal ratio, there is a
paucity of epidemiological data on domestic animals in Ghana. Several zoonotic diseases have
been reported in Ghana, including rabies, toxocariasis, toxoplasmosis, Q-fever, hepatitis E and
brucellosis. Risk factors such as close contact with animals, poor hand hygiene, poor sanitation,
and unvaccinated, free-ranging animals have been linked with zoonotic transmissions. Zoonoses
have been recorded in homes, slaughterhouses, and on farms in farm workers, butchers, and
vulnerable groups, including children, pregnant women, and HIV patients. A ‘One-Health’
approach, which comprises well-coordinated activities of both health and veterinary services, will
facilitate timely diagnosis and effective control of zoonoses in Ghana.
Review Article

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
18
Keywords: Zoonotic risks; domestic animals; Zoonoses; livestock population.
1. INTRODUCTION
Animals are kept in Ghanaian homes for both
personal and commercial purposes. Dogs and
cats are kept for companionship, breeding
purposes, and security, while ruminants and
poultry are bred to supplement family income
and provide food [1,2]. Globally, livestock
production is increasing to meet the ever-growing
demand for animal protein. Increase in both
human and livestock populations have
implications for transmission of zoonotic
diseases, as it allows for more frequent
interactions between the two within a limited
space [3,4]. Such close associations pose a
threat to public health, particularly in developing
countries with poor animal husbandry practices.
The fact that zoonoses account for more than
60% of all human diseases worldwide [3] further
highlights the need to limit human-animal
interactions.
Contact with animal fur/hair, excrement and the
use of animal droppings as farm manure are
some possible sources of infections [5].
According to health reports, most emerging/re-
emerging infectious diseases are of zoonotic
origin [6,7], with recent pandemics (COVID-19,
H1N1, H5N1 & Ebola Virus Disease) all affirming
this assertion [8]. Data from parts of the country
have reported multiple zoonotic agents in
domestic animals [1,9-11], coupled with poor
animal management practices by owners who
lack adequate knowledge of animal care. Given,
the frequent movement of people, animals, and
animal products, diseases can spread rapidly
across the globe [12]. A collaborative,
multisectoral approach under a ‘One-Health’
concept is therefore needed to prevent the
occurrence of future pandemics. In this write-up,
the zoonotic risks associated with keeping
domestic animals are discussed.
2. TYPES OF ANIMALS KEPT
A wide array of animals such as dogs, cats,
poultry, pigs, and ruminants are kept in
Ghanaian homes. Dogs and cats serve as pets,
biological control agents for rodents, also used in
hunting, and/or for security. The population of
dogs in urban areas is increasing because of
security concerns [13]. Other animals like poultry,
pigs, and ruminants are kept largely for
commercial purposes. The frequency and
distribution of these domestic animals vary from
place to place, with the availability of space,
income levels, and religious beliefs all influencing
the types of animals kept [14]. For instance, in
Islamic communities/homes, dogs and pigs are
not reared, although they favor keeping of sheep,
goats, and cows, which they mostly use for their
religious celebrations.
2.1 Animal Husbandry Practices
Three types of housing styles are employed by
animal owners. These are intensive, semi-
intensive, and extensive systems. Of the three,
only the intensive system ensures strict
confinement of animals, yet this is the least
practiced as it is more capital intensive. This
suggests that most animal owners allow their
animals to be nomadic within the communities,
polluting the environment through indiscriminate
defecation.
Owing to financial constraints, smallholder
farmers/ animal owners tend to raise their
animals under makeshift structures, some of
which are; sheds, yards, stalls and shades, and
feed their animals off household wastes or allow
them to scavenge for food. Meanwhile,
commercial farmers often house their animals in
a permanent shelter, where they provide
concentrates to bolster productivity [15].
Generally, deworming and vaccination of animals
are poor among smallholder farmers. This is
evident from helminthiasis accounting for a third
of losses of small ruminants and the spikes in the
incidence of rabies nationwide. Poor husbandry
practices and lack of treatment of animals aid
zoonotic transmissions from animals to humans
[16].
2.2 Policies on Domestic Animals,
Availability of Animal Hospitals and
Diagnostic Tools
Sources of animals may include family/friends,
breeding stations, open markets [15] and farms.
Others may acquire animals through the
adoption of stray animals or theft. Animals
introduced into homes are often of unknown
health status and there is rarely any form of
rigorous medical screening by veterinary officers,
preceding purchase. As such the purchase of
animals may introduce zoonotic agents into
homes/herds. Lack of strict confinement of these
animals in our communities further exacerbates
the risk of zoonotic transmissions to the general
public.

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
19
Although there are policies governing the types
of animals permitted close to human settlements,
these are largely unenforced [4]. Compared to
best practices elsewhere, where all pets are
accompanied outside their homes, while animal
farms are sited further away from human
settlements, stray animals feature prominently in
our communities and on our streets. Although
large animal farms are mostly situated in rural
areas, functional animal laboratories and clinics
are non-existent in these settings. Laboratory
facilities in the urban centers, however, lack
adequate diagnostic tools which also affects the
timely detection and management of diseases.
For instance, in the diagnosis of helminthiasis
microscopy remains the conventional method in
these animal clinics. Such tests, however, have
low specificity, considering similarities between
the ova of parasite species. Therefore, infections
may be misdiagnosed and/or underestimated.
Additionally, there remains a paucity of data on
the efficacy of drugs used in the treatment of
these animals. Considering the wide array of
domestic animals kept, epidemiological studies
are needed to protect both public and animal
health.
3. ZOONOTIC INFECTIONS IN DOMESTIC
ANIMALS
3.1 Zoonotic Transmissions from
Companion Animals
Dogs are among the most commonly kept
animals in Ghanaian homes. These animals cut
across all social classes and are found in all
types of settlements. More than 70% of the dogs
in Ghana are kept for security reasons, with a
similar proportion of these animals being allowed
to roam about freely within the communities [1,
17]. Dogs also serve commercial purposes as
they are sold as pets or for food. In some parts of
the country, dog markets are well-established
and these animals serve as a delicacy for many
[18].
One of the most commonly reported zoonoses in
dogs in Ghana is rabies, a viral disease with a
high fatality rate [2]. Human infections occur
primarily through dog bites. In addition to the
injury, pain, and trauma which often accompany
the bites, victimsmay also experience
hypersalivation, hyperventilation, hydrophobia,
fever, headaches, and aggression. Ghana has
initiated several campaigns in the past to curb
rabies, with a seemingly lack of well-coordinated
surveillance between public health and
veterinary services [19]. Scarcity of human
vaccines and immunoglobins [20], high cost of
vaccines [21], the indifference of dog owners,
and cultural beliefs towards vaccination have all
contributed to failed attempts in the past at
reducing rabies-related morbidity. In Ghana,
more than half of human-rabies cases result from
stray dog bites [22], indicating the need for
stricter enforcement of policies on pet keeping.
Reports of spikes in rabid bites country-wide [23]
suggest increasing dog-human contact, lack of
confinement, and poor vaccination practices
among owners. Mass canine vaccination is key
to meeting the Global Target of “zero human
rabies deaths” by 2030 [24]. However, with less
than 30% of dogs in the country vaccinated,
increased dog roaming population, and high dog
to a household-human ratio [9], Ghana appears
to be missing out on this target.
Apart from rabies, free-ranging dogs are likely to
transmit multiple zoonotic parasites, including
Toxocara canis, Ancylostoma caninum,
Diphyllobothrium latum, and Dipylidium caninum.
Of these, Toxocara canis and A. caninum are the
most frequently reported parasites of both
veterinary and public health importance.
Human toxocariasis occurs through the ingestion
of embryonated Toxocara eggs, with the passing
out of parasite-infested excreta by free-ranging
dogs facilitating transmission. Apart from dogs
and cats, the main biological transmitters of
toxocariasis, zoonotic transmission of
toxocariasis is possible through the consumption
of pig or poultry viscera [25]. Human infections
are usually classified into three forms (visceral
larva migrans, ocular or covert toxocariasis), with
the severity of disease based on the part of the
body infected. Worldwide, the varying prevalence
of Toxocaracanis have been reported, at less
than 50% in Europe and the Americas, and over
50% in Africa [26]. A study on human
toxocariasis in Ghana reported a prevalence of
53.5% in children, with pet keeping, geophagia,
and poor hand hygiene being significant risk
factors [26]. Cases of human infections in Ghana
may be underestimated given that serological
tests that offer accurate results with high
sensitivity and specificity [27] are not available in
the rural areas where infection rates are
significantly higher. The presence of Toxocara
eggs in vegetable farm soils suggests that
consumption of unwashed, fresh vegetable
products may be a source of infections [28].
Contact with the hair of dogs may also be a
mode of transmission of toxocariasis [29,30].

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
20
Table 1. Summary of studies on zoonotic infections in Ghana highlighting study location, transmitting animals and key findings
Author Year Study category Location Microbe/ disease Animals
involved
People
Involved
Key findings Ref.
Number
Adomako et al 2018 Retrospective review Eastern Region Rabies Dogs Rabies
victims
Most cases of rabid bites in
children under 10 years
Lack of collaboration between
health and veterinary services in
management of rabies
[19]
Adu 2017 Epidemiology Lower Manya-
Krobo, Eastern
region
Cooperia spp., Haemonchus
spp., Hookworms and
Trichostrongylus spp.
Cattle Recovery of four genera of
helminths
Hookworms and Trichostrongylus
identified as predominant helminth
species on farms
Possible bovine, zoonotic
transmission to humans
[11]
Amemor et al 2016 Epidemiology
North Tongu,
Volta region
Mycobacteriumbovis
Cattle Herdsmen Prevalence of 19% of BTB in cattle
Only cows were infected with BTB,
but no infection in bulls
Significant association between
seropositivity in cows and kraal
density
[44]
Amissah-
Reynolds
et al
2016 Epidemiology Mampong-
Ashanti
Toxocara canis, Dipylidium
caninum and Diphyllobothrium
latum
Dogs Dog owners Presence of zoonotic parasites in
dogs
Age of dog and location as
significant risk factors of infection
High number of stray dogs,
Poor pet management, lack of
vaccination and knowledge on
zoonosis
[1]
Amissah-
Reynolds
et al
2020 Epidemiology
Mampong-
Ashanti
Toxocaracanis, Fasciola spp. N/A N/A Risk of zoonotic transmission from
consumption of fresh vegetables
and salads
Zoonotic parasites in farm soils
and irrigation water
[28]

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
21
Author Year Study category Location Microbe/ disease Animals
involved
People
Involved
Key findings Ref.
Number
Antwi et al 2018 Seroepidemiology Kumasi Toxoplasmagondii Goats First report of toxoplasmosis in
goats
Nearly half (42%) of goats infected
Higher infections in males and
adults
[60]
Arko-Mensah 2000 Seroepidemiology Ghana Toxoplasma gonidii Pigs National prevalence of 39% in pigs
Seroprevalence varies with
ecological zone
[61]
Asante et al 2016 Descriptive survey Greater Accra
Region
HPAI H5N1 Poultry Outbreak of strain possibly from
Nigeria
Frequent movement of humans
and birds across the border
implicated in the outbreak
[68]
Asare et al 2019 Case report
Elmina Dipylidiumcaninum Pregnant
woman
Report of zoonotic dipylidiasis in a
pregnant woman
[31]
Awuni et al 2019 Descriptive survey
Upper East
Region
Rabies Dog owners Knowledge of rabies associated
with sex, occupation, educational
level and district of residence of
owners
District of residence, educational
level, knowledge on rabies,
occupation and religion were
associated with canine rabies
vaccination
[21]
Ayim-Akonor 2020 Risk analysis
Ghana Poultry zoonosis Poultry
farmers
Limited knowledge on zoonotic
poultry diseases
Poor attitudes towards use of
PPEs
Raising of multiple species may
allow for animal to animal
transmissions
[37]
Bentum et al 2019 Seroepidemiology Kumasi Toxoplasma gondii Sheep and
goats
Consumption of raw/undercooked
meat products from goats and
[59]

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
22
Author Year Study category Location Microbe/ disease Animals
involved
People
Involved
Key findings Ref.
Number
sheep can be a source of zoonotic
toxoplasmosis
Folitse et al 2014 Epidemiology Dormaa and
Kintampo
Districts
Tuberculosis and Brucellosis Cattle Increase in infection rates of both
diseases with age
[43]
Folitse et al 2020 Seroepidemiology Kumasi Coxiellaburnetii Small
ruminants
Higher risks in goats than in sheep
Risk of infections to abattoir
workers
[40]
Jarikre et al 2015 Seroepidemiology Northern,
Ashanti &
Greater Accra
Regions
Brucellosis Sheep and
goats
Female animals appear more
susceptible to infections
Higher infection rates in Ashanti
compared to two other regions
[42]
Johnson et al. 2015 Epidemiology Greater Accra
Region
Dogs Dog owners Increasing dog population in urban
areas for security reasons
Presence of zoonotic agents in
dogsPoor pet management
practices
[17]
Johnson et al. 2016 Epidemiology Greater Accra
Region
Cordylobia
anthropohaga,Dermatobia
hominis
Dogs Two species of insects identified
as cause of myiasis
Possibility of dog to human myiasis
transmission
[13]
Johnson et al 2019 Seroepidemiology Volta Region Coxiella burnetii Cattle, sheep
and goats
Farm workers Seropositivity rate of 21.6% in
ruminants
No knowledge of Q-fever by farm
workers and veterinary technical
staff
Risk of infections in children who
assist in farm activities
Q-fever is a possible cause of
abortions in animals
[49]
Kobbe et al 2008 Sero-epidemiology Ashanti Region Q-fever Children Early exposure of children to C.
burnetii.
[52]

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
23
Author Year Study category Location Microbe/ disease Animals
involved
People
Involved
Key findings Ref.
Number
Possible overestimation of malaria
given similar clinical manifestations
Kubuafor 2000 Seroepidemiology
Akwapim South Brucellosis Cattle Humans Age of animal is a significant risk
factor
Brucellosis implicated in abortion
and placental retention in cows
[46]
Kyei et al 2015 Seroepidemiology
Central Region Toxocariasis Children Higher infection rates in rural
areas,
Age, educational level, pet
keeping, geophagia and hand
washing with soap as significant
risk factors of infection
[26]
Laryea et al 2017 Review Kumasi Rabies Dogs Humans Stray dogs accounted for more
than half of dog bites
100% case fatality from rabid dog
bites
No post-exposure prophylaxis for
one-third of patients who reported
to health facilities
[22]
Majekodunmi
et al
2019 Seroepidemiology Greater Accra &
Upper East
regions
Hepatitis E virus, Taenia solium
and Trichinella spiralis
Pigs Pig handlers,
General
public
Regional variation in infection
rates,
High infection rates in pig handlers
compared to other community
members in Accra
Possible pig-related zoonoses
transmission along the pork value-
chain
[4]
Otupuri 2000 Descriptive survey
Kumasi Brucellosis,
Tuberculosis
Cysticercosis
Fascioliasis
Mange
Butchers Frequent detection of zoonotic
diseases at slaughterhouse
Unsafe meat handling practices by
butchers
Lack of formal training of butchers
General belief that religion confers
[74]

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
24
Author Year Study category Location Microbe/ disease Animals
involved
People
Involved
Key findings Ref.
Number
protection from contracting
infections
Owusu 2015 Sero-epidemiology Greater Accra
Region
Babesia spp. Dogs, cattle Malaria
patients
Possible zoonotic transmission for
dogs and cattle
Possible misdiagnosis of
Babesiosis as malaria
[32]
Punguyire et al
2017 Review Techiman Rabies Dogs Humans 100% case fatality from rabid dog
bites
Nearly half of dog bites among
children aged 1-15 years
[2]
Squire et al 2013 Epidemiology
Southern Ghana Cryptosporidium parvum Cattle Farmers Possible bovine transmission of
Cryptosporidium to humans and
other animals
Infection rates varies with type of
vegetation zone
[56]
Squire et al 2018 Epidemiology
Coastal
savannah zone,
Ghana
Gastrointestinal helminths ruminants Farmers Possible zoonotic transmission of
cryptosporidiosis from livestock
[10]
Turkson and
Boadu
1992 Epidemiology Coastal
savannah zone,
Ghana
Brucellosis Cattle Overall prevalence of 9.3%
Significantly higher infections in
older animals compared to
younger ones
[41]

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
25
Dipylidium caninum and Diphyllobothrium latum
are other parasites of zoonotic importance, with
the latter being a fish tapeworm [31]. A case of
human dipylidiasis has been reported in Ghana
[31], with infections of this zoonotic parasite
rarely encountered worldwide. Dogs have also
been implicated in the possible transfer of
myiasis to humans, with two species of insects
(Cordylobia anthropohaga, and Dermatobia
hominis) identified as causative agents of the
disease in dogs in the Greater Accra Region of
Ghana [13]. Canine transmission of Babesia is
also possible as dogs living in proximity to
humans have been found to be positive for the
pathogen [32]. Dogs may also aid in the
transmission of Ascaris lumbricoides as they
have been found to harbor viable eggs of the
parasite elsewhere [33], though this is yet to be
reported in Ghana. Dogs as companion animals,
share closer bonds with humans compared to
other domestic animals. Therefore, strict
confinement and regular treatment/vaccination of
these animals form a vital part of the
management of zoonotic diseases in Ghana.
Like dogs, cats are closely related to humans
and have been implicated in the transmission of
rabies, toxocariasis, and toxoplasmosis.
However, there is no study on feline infections
nor the role they play in zoonotic transmissions in
Ghana.
3.2 Zoonotic Transmissions from
Ruminants
Ruminants are another class of domestic animals
kept by Ghanaians. Goats, sheep, and cattle are
the main ruminants kept, providing income,
employment, and a major source of animal
protein [34]. To date, animal protein remains the
largest source of protein in Ghana [35]. With
Ghana’s domestic production falling below FAO
recommended levels, it is imperative to bolster
meat production. However, a myriad of problems
faced by farmers/animal owners hampers the
realization of this objective. Financial constraints
are the major challenges faced by farmers, as
they cannot afford the high cost of drugs,
feedstuffs, and adequate shelter for their animals
[36]. In addition, diseases (including
helminthiasis) and theft also account for a
significant amount of animal losses. To avert
economic losses resulting from theft [36], animal
owners keep their livestock in proximity to their
residence to ensure effective monitoring [37], a
condition that may aid zoonotic transmissions. In
Ghana, management practices and productivity
of ruminants vary from place to place. However,
an extensive system where animals are allowed
free movements in search of food and water is
the most practiced [35], creating ideal conditions
for human-animal contact and allowing for the
transfer of infections.
The strongylids (Trichostrongylus and
Haemonchus) and Fasciola are among the
zoonotic parasites that have been recovered
from ruminants in Ghana [38], with a higher
prevalence of nematode infections compared to
trematode infections. A recent molecular
characterization of Trichostrongylus infections in
ruminants suggested zoonotic transmission of
these parasites to humans [10]. In the absence
of molecular diagnosis, these infections could
easily have been diagnosed as hookworm
infections, considering the similarity between ova
of these parasites and the fact that human
trichostrongyliasis is rarely reported.
Bovine brucellosis and tuberculosis are two of
the world’s major zoonotic diseases [39].
Brucella spp and Mycobacterium bovis
respectively are the causative agents primarily
affecting cattle [40]. Brucellosis has been
reported in both large [41] and small ruminants
[42,43] in Ghana. The free movement of
ruminants increases the chances of infections. In
Ghana, ruminant diseases remain a public health
concern with close contact with infected animals
being the major risk factor [44]. Their occurrence
not only raise public health concerns but also
have a serious economic impact on producers,
regional and national economies through
decreased productivity and trade loss [45]. The
low endemicity of these diseases [46] does not
translate to their absence and hence policies that
check the unrestricted movements of ruminants,
continuous veterinary practices, and good
husbandry practices are needful for preventing
infections.
Bovine tuberculosis remains a major public
health problem in many sub-Saharan African
countries like Ghana. Currently, the National
Tuberculosis Control Programme focuses on
case management in human populations,
excluding the animals [47]. The increase in the
population of ruminants and the frequent
movement of livestock of unknown health status
across our borders may support the transmission
of bovine tuberculosis in Ghana. The fact that
“post-mortem inspection of carcasses for lesions”
remains the most widely diagnostic procedure is
also a means of transmission particularly in
densely populated areas, where animal-human
contact is more frequent [47]. Seropositivity in

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
26
cattle has been associated with kraal density
[43].
Free-roaming ruminants become exposed to
numerous pathogenic agents through what they
consume while on the move. Zoonoses such as
Anthrax [48], Q fever (Coxiella burnetii,
leptospirosis (Leptospira species), rickettsioses
(Rickettsia species), bartonellosis (Bartonella
species), plague (Yersinia pestis), rift valley fever
and chikungunya (arboviruses) are other
diseases they can transmit. Small ruminants
have been linked with the outbreak of Q fever in
the Volta region of Ghana [49]. Q fever, a
zoonotic disease caused by Coxiella burnetii,
which is able to cause abortions in livestock and
febrile illness in humans [49]. Studies have
shown that there is an exceptionally high
concentration of pathogenic agents at the time of
parturition [50,51], suggesting possible
transmission during handling of newborns,
placental tissues, and amniotic fluids. The
closeness of these ruminants to human
settlements increases the rate of infection to the
disease. Reports of Q-fever in children suggests
the possibility of overestimation of malaria cases
in Ghana, considering similar clinical
manifestations of the two disease and the low
knowledge on Q-fever infections [52].
Another zoonotic parasite recovered from
ruminants in Ghana is Cryptosporidium parvum
[53]. This parasite is an enteric protozoan noted
for causing diarrhoea. Apart from breastfeeding,
infections are transmissible through food, water,
or soil containing oocysts- the infective stage of
the parasite [54]. Indiscriminate defecation or
disposal of animal excreta into water bodies
could also introduce infections into the food
chain. Other risk factors of infection include lack
of potable water and toilets, overcrowding
(especially in slums), and animal contact [55]. A
study on Cryptosporidium infections in cattle from
Southern Ghana revealed an overall prevalence
of 29.0%, with infection rates varying according
to vegetation zones [56]. The study further
highlighted the possibility of zoonotic
transmissions between farmers and their
livestock. The use of untreated animal excreta as
manure on vegetable farms could also aid in the
transmission of cryptosporidiosis.
Toxoplasmosis, caused by the protozoan
parasite T. gondii, is an important zoonosis
worldwide. In Ghana, there are numerous reports
of human infections (including pregnant and HIV
patients) [57,58], but very little information on
animals. Human infections result from the
ingestion of raw foods (meat, vegetables, and
fruits) and soil containing sporulated oocysts.
Transmission through organ transplantation,
blood transfusion as well as congenital
transmissions have also been reported. With
varying prevalence reported globally, pet-
keeping, contact with soil and consumption of
unpasteurized dairy products, and unwashed
fruits and vegetables have been identified as
significant risk factors. So far, small ruminants
[59,60] and pigs [61] are known reservoirs of the
parasite in Ghana. Although cats have been
implicated in the spread of the disease in Ghana
[58], there is no available report on
toxoplasmosis in these companion animals.
Most of these zoonoses from ruminants are
known to pose considerable challenges in their
diagnosis as they share common symptoms with
many infectious diseases [62]. For this reason,
many of these zoonoses of public health concern
appear understated, thereby limiting awareness
of clinicians and policymakers. Additionally, the
lack of adequate laboratory facilities hampers
management efforts. Best preventive measures
which include good animal husbandry, veterinary
routines, grazing management, and personal
hygiene [63] are paramount in protecting both
animal and public health.
3.3 Zoonotic Transmissions from Pigs
Pig production is gaining prominence in the
livestock production industry owing to the high
prolificacy rate, short generational time, and the
relative ease of management of these animals
[64]. Globally, meat production has more than
quadrupled over the past six decades, with pork
as the leading source of animal protein [65].
Ghana has also seen a proliferation of pig farms
(both commercial and smallholder pig
production) as a result of increasing demand for
animal protein in the country. Though there are
by-laws prohibiting the raising of pigs near
human settlements, it is not uncommon to find
pigs in homes or roaming about in some
communities [4]. With these animals feeding off
anything they come across, free-ranging pigs
that come into contact with human excreta can
aid in the transmission of zoonosis. A study on
toxoplasmosis in Ghana identified pigs as
possible biological transmitters of the disease
[61]. The study reported a national prevalence of
39% in pigs, with age and breed of pigs,
environmental conditions, and management
practices as significant risk factors. The recovery
of Taeniasolium, Trichinella, and Hepatitis E
Virus (HEV) from pigs in Ghana suggests

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
27
possible zoonotic transmissions to humans
through the ingestion of raw or undercooked
pork. Pregnant women are particularly vulnerable
with the risk of stillbirths from hepatitis E
infections [66], or possible congenital
transmission of toxoplasmosis to their children
[57,58]. This calls for urgent attention and
regulation by relevant stakeholders.
3.4 Zoonotic Transmissions from Poultry
The poultry industry contributes substantially to
animal protein worldwide, second only to pork as
the leading source of animal protein. These birds
are mainly kept for their eggs and/or meat, while
their droppings may serve as sources of farm
manure. Competitive pricing and the absence of
cultural or religious prohibitions on consumption
make chicken an attractive option to consumers
as compared to other animals [67]. Attempts to
increase productivity amidst the growing demand
for animal protein is often met with constraints,
including diseases. A number of zoonotic poultry
diseases have been recorded in Ghana,
including highly pathogenic avian influenza
(HPAI) virus subtype H5N1, Newcastle disease,
Salmonellosis, and Coccidiosis [68-71]. Poor on-
farm attitudes and practices increase the risk of
human infections with zoonotic poultry diseases
[37].
3.5 Zoonotic Transmissions from Rabbits
And Grass Cutters
In addition to the aforementioned animals,
rabbits and grass cutters are also kept in some
households, though on a small-scale. These
animals are kept under strict confinement,
limiting contact with their caregivers or owners.
Several pathogens have been recovered from
grasscutters, including Trichomonas spp, Giardia
spp, Eimeria spp., Ancylostoma sp., and
Schistosoma haematobium, with no available
information on zoonosis [72,73]. Zoonotic
infections from these animals may stem from
improper cooking of meat or contact with their
feces. Hunting for wild game and domestication
of wild species of animals like grass cutters may
be a source of zoonotic transmissions from the
wild.
4. ROLE OF SLAUGHTERHOUSES,
BUTCHERS, FOOD VENDORS AND
NOMADIC HERDSMEN IN TRANSMIS-
SION OF ZOONOSIS
Apart from keeping live animals close to human
settlements, zoonotic diseases are also
transmissible from meat products bought from
food vendors, meat shops, and slaughterhouses.
Slaughterhouses play a critical role in the food
industry, contributing to the alleviation of protein
malnutrition while providing employment for
several others, including butchers. As such
proper surveillance and surveys on
slaughterhouse activities are needful to avert
transmission of zoonotic diseases to the public
through improvement in the detection and
management of diseases. Rigorous ante- and
post-mortem inspections are also vital in
protecting the health of patrons. Reports of
failure of butchers to adhere to safety protocols
and precautionary measures as a result of
ignorance, indifference, or religious beliefs are a
source of concern [74]. It is therefore
unsurprising that zoonotic infections such as
brucellosis have been reported in
slaughterhouse workers in Ghana [75]. Regular
training and formulation of laws are needed to
limit community-spread of zoonoses from
slaughterhouses.
The activities of nomadic herdsmen who herd
their flock (mainly cattle) close to human
settlements may also be a source of zoonotic
transmissions. Indiscriminate defecation as these
animal graze tends to release enteric zoonotic
agents into the environment. Like farmers, these
herdsmen have regular, close contact with the
animals, a risk factor for transmission of most
zoonotic infections. Activities of chop bar
operators and other intermediaries involved in
the sale or processing of meat products should
also be well regulated to avert transmission of
infections along the food chain.
5. CONCLUSION
Ghana has seen an increased household-
human-animal ratio over the past few decades.
Lack of confinement of unvaccinated animals
which are harboring zoonotic agents is ideal for
the transmission of zoonoses to humans. Lack of
adequate laboratory facilities and lack of
coordination between health and veterinary
services affects the timely diagnosis of infections.
A One-Health approach is needed for effective
control of zoonoses in Ghana.
6. RECOMMENDATIONS
Epidemiology data on populations of animals,
management practices and zoonotic diseases
nationwide to inform control strategies.
Formulation and enforcement of policies and by-
laws on pet keeping and livestock production,

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
28
particularly near human settlements are needed
to prevent zoonotic transmissions. National
Control Programmes for diseases like TB should
include the management of disease in animal
populations. Management of zoonosis should
include well-coordinated efforts between health
and veterinary services to ensure timely
diagnosis and management of diseases.
COMPETING INTERESTS
Author has declared that no competing interests
exist.
REFERENCES
1. Amissah-Reynolds PK, Monney I, Adowah
LM, Agyemang SO. Prevalence of
helminths in dogs and owners’ awareness
of zoonotic diseases in Mampong, Ashanti,
Ghana. Journal of Parasitology Research.
2016.
2. Punguyire DT, Osei-Tutu A, Aleser EV,
Letsa T. Level and pattern of human rabies
and dog bites in Techiman Municipality in
the Middle Belt of Ghana: a six year
retrospective records review. Pan African
Medical Journal. 2017;28(1).
3. Klous G, Huss A, Heederik DJ, Coutinho
RA. Human–livestock contacts and their
relationship to transmission of zoonotic
pathogens, a systematic review of
literature. One Health. 2016;2:65-76.
4. Majekodunmi AO, Addo HO, Bagulo H,
Bimi L. Integrated value-chain and risk
assessment of Pig-Related Zoonoses in
Ghana. PloS one. 2019;14(11).
5. Conrad CC, Stanford K, Narvaez-Bravo C,
Callaway T, McAllister T. Farm fairs and
petting zoos: A review of animal contact as
a source of zoonotic enteric disease.
Foodborne pathogens and disease.
2017;14(2):59-73.
6. Taylor LH, Latham SM, Woolhouse ME.
Risk factors for human disease
emergence. Philosophical Transactions of
the Royal Society of London Series B:
Biological Sciences. 2001;356(1411):983-
9.
7. Gebreyes WA, Dupouy-Camet J, Newport
MJ, Oliveira CJ, Schlesinger LS, Saif YM,
et al. The global one health paradigm:
challenges and opportunities for tackling
infectious diseases at the human, animal,
and environment interface in low-resource
settings. PLoS neglected tropical diseases.
2014;8(11).
8. Ahmad T, Khan M, Haroon THM, Nasir S,
Hui J, Bonilla-Aldana DK, et al. COVID-19:
Zoonotic aspects. Travel Medicine and
Infectious Disease; 2020.
9. Tasiame W, Johnson S, Burimuah V,
Akyereko E, Amemor E. Dog population
structure in Kumasi, Ghana: a missing link
towards rabies control. The Pan African
Medical Journal. 2019;33.
10. Squire SA, Yang R, Robertson I, Ayi I,
Squire DS, Ryan U. Gastrointestinal
helminths in farmers and their ruminant
livestock from the Coastal Savannah zone
of Ghana. Parasitology Research. 2018;
117(10):3183-94.
11. Adu AK. Cattle as Potential Reservoir for
Parasitic Zoonotic Diseases in the Lower
Manya Krobo District in the Eastern
Region of Ghana: University Of Ghana;
2017.
12. CDC. One Health; 2018.
Available:https://wwwcdcgov/onehealth/ba
sics/
13. Johnson SA, Gakuya DW, Mbuthia PG,
Mande JD, Afakye K, Maingi N. Myiasis in
dogs in the Greater Accra Region of
Ghana. Vector-Borne and Zoonotic
Diseases. 2016;16(1):54-7.
14. Symons L. Agricultural geography:
Routledge; 2019.
15. Dodua ASN, Richard O-A, Dennis AO,
Kwadjo AB, Matthew SB, Anne SC.
Production practices of local pig farmers in
Ghana; 2019.
16. Voss K. Public Health Risk in Animal
Shelters. 2019.
17. Johnson SAM, Gakuya DW, Mbuthia PG,
Mande JD, Maingi N. Prevalence of
gastrointestinal helminths and manage-
ment practices for dogs in the Greater
Accra region of Ghana. Heliyon. 2015;
1(1):e00023.
18. Fuseini A, Sulemana I. An Exploratory
Study of the Influence of Attitudes toward
Animal Welfare on Meat Consumption in
Ghana. Food Ethics. 2018;2(1):57-75.
19. Adomako B-Y, Baiden F, Sackey S,
Ameme DK, Wurapa F, Nyarko KM, et al.
Dog Bites and Rabies in the Eastern
Region of Ghana in 2013–2015: A Call for
a One-Health Approach. Journal of tropical
medicine;2018.
20. Laryea D, Kyem G, Awittor F, Amoako YA,
Owusu R, editors. Scarcity of the rabies
vaccine and immunoglobulin: A potential
for rabies outbreak in Ghana. APHA 2016

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
29
Annual Meeting & Expo. American Public
Health Association; 2016.
21. Awuni B, Tarkang E, Manu E, Amu H,
Ayanore MA, Aku FY, et al. Dog Owners’
Knowledge about Rabies and Other
Factors That Influence Canine Anti-Rabies
Vaccination in the Upper East Region of
Ghana. Tropical medicine and Infectious
Disease. 2019;4(3):115.
22. Laryea DO, Ofori RO, Arthur J, Agyemang
EO, Spangenberg K. Human Rabies in
Kumasi: A Growing Public Health Concern.
African Journal of Current Medical
Research. 2017;1(1).
23. WHO. Spread of canine rabies sparks
broad community response in Ghanaian
townSpread of canine rabies sparks broad
community response in Ghanaian Town;
2019.
Available: https://www.who.int/news-
room/feature-stories/detail/spread-of-
canine-rabies-sparks-broad-community-
response-in-ghanaian-town.
24. WHO. Global elimination of dog-mediated
human rabies: report of the rabies global
conference, 10-11 December 2015,
Geneva, Switzerland. World Health
Organization; 2016.
25. Taira K, Saeed I, Permin A, Kapel C.
Zoonotic risk of Toxocara canis infection
through consumption of pig or poultry
viscera. Veterinary Parasitology. 2004;
121(1-2):115-24.
26. Kyei G, Ayi I, Boampong J, Turkson P.
Sero-epidemiology of Toxocara canis
infection in children attending four selected
health facilities in the central region of
Ghana. Ghana medical journal. 2015;
49(2):77-83.
27. Nunes CM, Tundisi RN, Heinemann MB,
Ogassawara S, Richtzenhain LJ.
Toxocariasis: serological diagnosis by
indirect antibody competition ELISA.
Revista do Instituto de Medicina Tropical
de São Paulo. 1999;41(2):95-100.
28. Amissah-Reynolds PK, Yar DD, Gyamerah
I, Apenteng OY, Sakyi S. Fresh
Vegetables and Ready-to-eat Salads:
Sources of Parasitic Zoonoses in
Mampong-Ashanti, Ghana. European
Journal of Nutrition & Food Safety. 2020;
47-55.
29. Semih Ö, Hatice Ö, Gönenç B, Özbakiş G,
Yildiz C. Presence of Toxocara eggs on
the hair of dogs and cats. Ankara
Üniversitesi Veteriner Fakültesi Dergisi.
2013;60(3):171-6.
30. Wael F, Holt HR, Tayel AA. Risk of
Toxocara canis eggs in stray and domestic
dog hair in Egypt. Veterinary parasitology.
2011;178(3-4):319-23.
31. Asare KK, Opoku YK, Anning AS, Afrifa J,
Gyamerah EO. Case Report: A case of
dipylidiasis in a first-trimester pregnant
woman attending a routine antenatal clinic
at Elmina health centre, Ghana. F1000
Research. 2019;8(857):857.
32. Owusu I. Detection of Zoonotic Babesia
Species in Greater Accra, Ghana:
University of Ghana; 2015.
33. Shalaby H, Abdel-Shafy S, Derbala A. The
role of dogs in transmission of Ascaris
lumbricoides for humans. Parasitology
research. 2010;106(5):1021-6.
34. Duku S, van der Zijpp AJ, Udo M.
Household vulnerability and small ruminant
benefits in the transitional zone of Ghana.
Journal of Agricultural Extension and Rural
Development. 2010;4(5):98-106.
35. Adzitey F. Animal and meat production in
Ghana-An overview. The Journal of
World’s Poultry Research. 2013;3(1):1-4.
36. Baah J, Tuah A, Addah W, Tait R. Small
ruminant production characteristics in
urban households in Ghana. Age (years).
2012;29(15):30-9.
37. Ayim‐Akonor M, Krumkamp R, May J,
Mertens E. Understanding attitude,
practices and knowledge of zoonotic
infectious disease risks among poultry
farmers in Ghana. Veterinary Medicine and
Science; 2020.
38. Amissah-Reynolds PK, Bonsu FRK, Yar
DD, Osei CP, Nuamah F, Ndego EA.
Trichostrongylus infections in slaughtered
Ruminants: The case of selected
slaughterhouses in Kumasi, Ghana.
Ghana Science Association, 31st Biennial
Conference book of Abstracts; 2019.
39. Boukary AR, Saegerman C, Abatih E,
Fretin D, Bada RA, De Deken R, et al.
Seroprevalence and potential risk factors
for Brucella spp. infection in traditional
cattle, sheep and goats reared in urban,
periurban and rural areas of Niger. PloS
one. 2013;8(12).
40. Folitse RD, Opoku-Agyemang T, Amemor
E, Opoku ED, Bentum KE, Emikpe BO.
Serological evidence of Coxiella burnetii
infection in slaughtered sheep and goats at
Kumasi Abattoir, Ghana. Journal of
Immunoassay and Immunochemistry.
2020;41(2):152-7.

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
30
41. Turkson P, Boadu D. Epidemiology of
bovine brucellosis in the Coastal Savanna
zone of Ghana. Acta tropica. 1992;
52(1):39-43.
42. Jarikre T, Emikpe B, Folitse R, Odoom T,
Fuseini A, Shaibu E. Prevalence of
brucellosis in small ruminants in three
regions of Ghana. Bulgarian J Vet Med.
2015;18:49-55.
43. Folitse R, Boi-Kikimoto B, Emikpe B,
Atawalna J. The prevalence of Bovine
tuberculosis and brucellosis in cattle from
selected herds in Dormaa and Kintampo
Districts, Brong Ahafo region, Ghana.
Archives of Clinical Microbiology. 2014;
5(2).
44. Amemor EA, Sackey SO, Yebuah N,
Folitse RD, Emikpe BO, Afari E, et al. The
prevalence of tuberculosis in cattle and
their handlers in north Tongu, Volta region,
Ghana. African Journal of Infectious
Diseases. 2017;11(1):12-7.
45. Otchere E, Okantah S. Smallholder dairy
production and marketing in Ghana.
Smallholder dairy production and
marketing—Opportunities and constraints.
2017;215.
46. Kubuafor D, Awumbila B, Akanmori B.
Seroprevalence of brucellosis in cattle and
humans in the Akwapim-South district of
Ghana: public health implications. Acta
Tropica. 2000;76(1):45-8.
47. Mwinyelle GB, Alhassan A. Overview of
bovine tuberculosis in Ghana. Zoonotic
Tuberculosis: Mycobacterium bovis and
Other Pathogenic Mycobacteria. 2014;175-
80.
48. Edward F, Osei-Tutu A, Gbeddy K,
Tsitsiwu J, Quist C. Anthrax outbreak at
disease investigation farm, Techiman,
Ghana, 2013. International Journal of
Infectious Diseases. 2014;21:145.
49. Johnson SA, Kaneene JB, Asare‐Dompreh
K, Tasiame W, Mensah IG, Afakye K, et al.
Seroprevalence of Q fever in cattle, sheep
and goats in the Volta region of Ghana.
Veterinary Medicine and Science. 2019;
5(3):402-11.
50. Costa SCL, de Magalhães VCS, de
Oliveira UV, Carvalho FS, de Almeida CP,
Machado RZ, et al. Transplacental
transmission of bovine tick-borne
pathogens: frequency, co-infections and
fatal neonatal anaplasmosis in a region of
enzootic stability in the northeast of Brazil.
Ticks and tick-borne diseases. 2016;
7(2):270-5.
51. Plummer PJ, McClure JT, Menzies P,
Morley PS, Van den Brom R, Van Metre
DC. Management of C oxiella burnetii
infection in livestock populations and the
associated zoonotic risk: A consensus
statement. Journal of veterinary internal
medicine. 2018;32(5):1481-94.
52. Kobbe R, Kramme S, Kreuels B, Adjei S,
Kreuzberg C, Panning M, et al. Q fever in
young children, Ghana. Emerging
infectious diseases. 2008;14(2):344.
53. Squire SA, Ryan U. Cryptosporidium and
Giardia in Africa: current and future
challenges. Parasites & vectors. 2017;
10(1):195.
54. Bouzid M, Hunter PR, Chalmers RM, Tyler
KM. Cryptosporidium pathogenicity and
virulence. Clinical microbiology reviews.
2013;26(1):115-34.
55. Bouzid M, Kintz E, Hunter PR. Risk factors
for Cryptosporidium infection in low and
middle income countries: A systematic
review and meta-analysis. PLoS neglected
tropical diseases. 2018;12(6):e0006553.
56. Squire SA, Beyuo J, Amafu-Dey H.
Prevalence of Cryptosporidium oocysts in
cattle from Southern Ghana. Veterinarski
arhiv. 2013;83(5):497-507.
57. Ayi I, Edu S, Apea-Kubi K, Boamah D,
Bosompem K, Edoh D. Sero-epidemiology
of toxoplasmosis amongst pregnant
women in the greater Accra region of
Ghana. Ghana medical journal. 2009;
43(3).
58. Kwofie KD, Ghansah A, Osei JHN,
Frempong KK, Obed S, Frimpong EH, et
al. Indication of risk of mother-to-child
Toxoplasma gondii transmission in the
Greater Accra Region of Ghana. Maternal
and Child Health Journal. 2016;20(12):
2581-8.
59. Bentum KE, Folitse RD, Amemor E,
Burimuah V, Opoku-Agyemang T, Emikpe
BO. Seroprevalence of Toxoplasma Gondii
antibodies in sheep and goats slaughtered
at the Kumasi Abattoir, Ghana. Journal of
Immunoassay and Immunochemistry.
2019;40(5):495-501.
60. Antwi P, Emikpe B, Essel K, Folitse R,
Jarikre T. Detection of Toxoplasma gondii
in goats at the Kumasi abattoir, Ghana.
International Journal of Infectious
Diseases. 2018;73:305.
61. Arko-Mensah J, Bosompem K, Canacoo E,
Wastling J, Akanmori B. The
seroprevalence of toxoplasmosis in pigs in
Ghana. Acta Tropica. 2000;76(1):27-31.

Amissah-Reynolds; IJPR, 4(3): 17-31, 2020; Article no.IJPR.57959
31
62. Halliday JE, Allan KJ, Ekwem D,
Cleaveland S, Kazwala RR, Crump JA.
One health: Endemic zoonoses in the
tropics: A public health problem hiding in
plain sight. The Veterinary Record. 2015;
176(9):220.
63. Pisseri F, De Benedictis C, Roberti di
Sarsina P, Azzarello B. Sustainable animal
production, systemic prevention strategies
in parasitic diseases of ruminants.
Alternative & Integrative Medicine; 2013.
64. Thornton PK. Livestock production: recent
trends, future prospects. Philosophical
Transactions of the Royal Society B:
Biological Sciences. 2010;365(1554):2853-
67.
65. Ritchie H, Roser M. Meat and dairy
production. Our World in Data; 2017.
66. Rein DB, Stevens GA, Theaker J,
Wittenborn JS, Wiersma ST. The global
burden of hepatitis E virus genotypes 1
and 2 in 2005. Hepatology. 2012;55(4):
988-97.
67. Valceschini E, editor Poultry meat trends
and consumer attitudes. Proceedings of
the XII European Poultry Conference;
2006.
68. Asante IA, Bertram S, Awuni J, Commey
ANO, Aniwa B, Ampofo WK, et al. Highly
pathogenic avian influenza A (H5N1) virus
among poultry, Ghana, 2015. Emerging
Infectious Diseases. 2016;22(12):2209.
69. Andoh LA, Ahmed S, Olsen JE, Obiri-
Danso K, Newman MJ, Opintan JA, et al.
Prevalence and characterization of
Salmonella among humans in Ghana.
Tropical medicine and health. 2017;
45(1):3.
70. Boakye O, Emikpe B, Folitse R, Bonnah S,
Adusei K, Owusu M, et al. Serological
detection of Newcastle disease virus
antibodies in local chickens and guinea
fowls in the area of Kumasi, Ghana.
Brazilian Journal of Poultry Science. 2016;
18(1):87-92.
71. Fornace KM, Clark EL, Macdonald SE,
Namangala B, Karimuribo E, Awuni JA, et
al. Occurrence of Eimeria species
parasites on small-scale commercial
chicken farms in Africa and indication of
economic profitability. PLoS One. 2013;
8(12).
72. Kankam T, Adu EK, Awumbila B.
Gastrointestinal parasites of the
grasscutter (Thryonomys swinderianus,
Temminck 1827) on the Accra Plains of
Ghana. African journal of ecology. 2009;
47(3):416-21.
73. Futagbi G, Agyei D, Aboagye I, Yirenya-
Tawiah D, Edoh D. Intestinal parasites of
the grasscutter (Thryonomys swinderianus
Temminck 1827) from the Kwaebibirem
District of the Eastern Region of Ghana.
West African Journal of Applied Ecology.
2010;17(1).
74. Otupiri E, Adam M, Laing E, Akanmori B.
Detection and management of zoonotic
diseases at the Kumasi slaughterhouse in
Ghana. Acta tropica. 2000;76(1):15-9.
75. Amegashie EA, Owusu-Dabo E, Salifu SP,
Afum-Adjei Awuah A, Baffour-Awuah S,
Addofoh N, et al. Sero-prevalence and
occupational risk factors for Brucella
infection among slaughterhouse workers
and butchers in Kumasi, Ghana; 2017.
© 2020 Amissah-Reynolds; This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any
medium, provided the original work is properly cited.
Peer-review history:
The peer review history for this paper can be accessed here:
http://www.sdiarticle4.com/review-history/57959