2 Oke
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One Health
journal homepage: www.elsevier.com/locate/onehlt
A R T I C L E I N F O A B S T R A C T
Keywords: The increasing frequency of spillover of zoonotic pathogens from animals to humans in recent years highlights a
One Health need to develop a more comprehensive framework to investigate and prevent pathogens of animal origin,
Qatar including rodents. Despite the presence of several species of rodents, there is a certain knowledge gap regarding
Rodent
rodent-borne zoonoses in Qatar. The current review provides an update on rodent-borne zoonoses in Qatar, its
Rodent-borne zoonoses
possible drivers and transmission dynamics, and proposed a One Health framework for intervention. Following
an extensive literature review, we conducted a field investigation. Then the qualitative information and
knowledge gaps were addressed with a virtual discussion with national, regional, and international experts in the
relevant field. Overall, Rattus norvegicus population was found to be more prevalent, followed by Rattus rattus,
and M. musculus, which are mainly found in animal farms, followed by agricultural farms, residential areas, and
other facilities. Over 50% of rodents carry at least one pathogen of public health importance. Several pathogens
were identified at the human, animal, and ecosystem interface, which can be mediated in transmission by ro
dents. E. coli, Salmonella spp., and Campylobacter spp. are the frequently reported bacteria. Hymenolepis spp.,
Cryptosporidium spp., Giardia spp., Entamoeba spp., and Toxoplasma spp. are the major parasites. In addition,
many vectors, including Ornithonyssus bacoti and Xenopsylla astia were reported in this country. Based on the
changes over the past 70 years in Qatar, seven drivers have been identified, which could be important in rodent-
borne disease emergences, such as the Oil and gas revolution, fast population growth, rapid urbanization,
importation of food and agricultural products, agricultural and livestock development, farm biosecurity, and
stray animals. The experts emphasized that mixed-species animal farming with poor biosecurity and manage
ment can be associated to increase the risk of zoonoses. Moreover, rapid urbanization and global climate change
together can alter the ecosystem of the country and impact on vectors and vector-borne diseases. Finally, the One
Health framework has been proposed for the surveillance, and mitigation of any future spillover or epidemic of
rodent-borne zoonoses.
1. Background mammalian world. These animals have high evolution abilities, such as
high prolificacy, short gestation period, robust body shape, and small to
Rodents are an essential component of every terrestrial ecosystem. medium-sized bodies that acclimatized them for surviving in different
With about 36 families and 2552 species, these animals are the most ecosystems [1], including deserts. They serve to land habitat ecosystems
diverse and highest representing (40% of the total mammals) in the by modification of the soil structure, increasing soil aeration and
* Corresponding author at: Department of Animal Resources, Ministry of Municipality, Doha, Qatar.
E-mail address: mmmohammed@mm.gov.qa (Md.M. Islam).
https://doi.org/10.1016/j.onehlt.2023.100517
Received 16 November 2022; Received in revised form 21 February 2023; Accepted 22 February 2023
Available online 26 February 2023
2352-7714/© 2023 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Md.M. Islam et al. One Health 16 (2023) 100517
hydration, energy and nutrition cycling, seed and spore pollination and 2.2. Field investigation
dispersal, and source of feed for other animals (eagle, fox, and cat) [1].
In addition, they cause significant harm, such as consuming, contami We conducted a cross sectional study starting from the year 2018 to
nating, and damaging our foods, destroying property (clothes and doc 2019 to assess presence of rodent-borne zoonotic pathogens in Qatar. As
uments) and structure (floor and networking facilities), and sometimes such, we trapped 148 rodents from some selected areas of the country
causing accidents (damage to the electrical network) [2]. These animals and conducted gross external examination, necropsy, coproscopy, his
also have serious concern of transmitting pathogens of public health topathology, bacterial culture and identification, ELISA, PCR, and
importance [3,4], and facilitating the transmission of at least 84 zoo sequencing to understand the zoonotic pathogens. Detail of the rodents
notic diseases as carriers or reservoirs [5]. The commensal rodents have and their related pathogens were described previously [17–19].
higher public health significance as they carry pathogens directly to
humans and other animals (livestock and pets) through contact with 2.3. Expert panel discussion
rodent feces, urine, and skin/fur and indirectly through ectoparasites
and other vectors [6]. There are several histories of rodent-borne zoo Subsequently, a One Health expert panel was held in September
notic disease epidemics globally, such as plague, leishmaniasis, and ty 2022 via Microsoft Teams to share information and address remaining
phus fever [7–10]. In recent years, the increasing frequency of spillover knowledge gaps. The panel was distributed into two sections based on
of zoonotic pathogens from animals highlights a need to develop a the availability of the experts who had been invited. A group of 27 ex
framework to investigate and prevent pathogens from rodents. perts attended the first meeting, whereas 14 experts were in the second
Qatar is a small peninsular Arab country, home to people from over session. The experts were from national, regional, and international
90 countries, most of whom are from South Asia. There are four species level in the fields of animal health, public health, or environment
of rodents reported in this country, one is the wild species: Jaculus jac department. Criteria for expert selection included: 10 years or more
ulus [11], and others are commensal species: Mus musculus, Rattus nor experience to work in public health, animal health, zoonotic disease,
vegicus, and Rattus rattus [11–14]. To prevent any rodent-related livestock or agricultural farm management, rodent control, rodent dis
zoonoses epidemic in the future in this country, especially during the ease research, national or international policy making in public health.
FIFA World Cup 2022, a study was conducted on commensal rodents and Additionally, minimum of 10 years residential experience within Qatar
rodent-borne pathogens. Several articles were published based on this context was also required. Both meetings were conducted in English
research [5,15–19], which suggest that rodent-borne zoonoses is not a language and lasted for at least one hour. One of the authors was
neglected issue. Therefore, intervention on such zoonoses needs to be assigned to be a moderator and recorded the meetings while the rest
emphasized. One Health is a multisectoral collaborative approach, were participants.
which is an essential component in combatting health issues at the During the meetings, a brief presentation was shared with the experts
human-animal-ecosystem interface. Applying this approach in preven which explained the research findings on rodent and rodent-borne
tion and control of zoonotic diseases can save lives, which also ensures zoonoses in Qatar. Afterwards, a list of challenges and knowledge gaps
an efficient use of resources (fund, facility, and personnel), and a quality was shared with the experts. These gaps included: increased the risk of
healthcare delivery in a timely manner. Despite increasing success and rodent-borne zoonoses in Qatar from imports of food and agricultural
awareness of the One Health approach, shortage of communication, products, role of immigrant workers in transmission of these diseases
coordination and structured guideline for the relevant sectors is still inside Qatar and cross-border transmission, impact of climate change
hindering implementation of this tactic [20]. The current review pro and urbanization in Qatar on rodent-borne disease transmission, man
vides an update of rodent-borne zoonoses in Qatar, as well as possible agement of rodents in traditional farming and old housing systems of the
drivers and transmission dynamics of such zoonoses. The present study country, and major risks of rodent-borne disease within the country.
also proposes a possible One Health intervention program to prevent Afterwards, the experts were asked to share possible interventions for
such zoonoses epidemics in this country. the aforementioned challenges using One Health approach. Finally, the
two meetings were transcribed and converted in a single document and
2. Materials and methods shared with the experts for verification.
Before the start of the review itself, the authors shared their 3.1. Overview of rodent-borne pathogens
knowledge and views with each other using Delphi Method to under
stand the rodent-borne zoonotic pathogens, their drivers, and trans Overall, R. norvegicus found to be more prevalent followed by
mission dynamics at Qatari ecosystem and culture. Then we conducted R. rattus, and M. musculus in Qatar [17] and mainly distributed in the
an extensive literature review for relevant articles published between animal farms, followed by agricultural farms, residential areas, and
2000 and middle of 2022 in Google scholar, PubMed, Science Direct, other facilities (commercial and industrial areas). Over 50% of rodents
Web of Science, and Scopus in terms of rodent-borne bacteria, virus, of Qatar carry at least one pathogen of public health importance [19].
helminths, protozoa, and vectors at the human, animal, and ecosystem
interface of Qatar [5,15,16]. We used Boolean operations for the key 3.1.1. Bacterial pathogens
words to enhance retrieval of relevant articles and narrow the search A total of 23 bacterial species were reported at the human, animal,
results. In addition, references of the selected articles were examined to and environment interface in Qatar (Table 1). The majority of them were
cover the related articles. We also conducted electronic and hand search found in humans and rodents. Campylobacter spp., Escherichia spp.,
for the grey literature related to Qatar population, economy, trade, and Salmonella spp. and Rickettsia spp. were reported in domesticated ani
development from different ministries of Qatar, including the Ministry mals, such as livestock, poultry, and pets. In addition, Campylobacter
of Public Health, Ministry of Municipality and Environment, and Qatar spp., Corynebacterium spp., and Escherichia spp. were notified from the
Statistical Authority, and international organizations, such as the World environment samples of the animal farms and live animal markets.
Bank, World Health Organization, and World Organization for Animal
Health. The associated citizen science documents were studied in the 3.1.2. Viral pathogens
blog posts, social media, and newspapers. Rodents can be involved in transmission of chikungunya and hepa
titis E, which have been reported among humans (Table 2). Additionally,
rabies was identified in both humans and animals. Evidence of
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Md.M. Islam et al. One Health 16 (2023) 100517
Table 1 Table 3
Rodent-borne zoonotic bacteria reported in Qatar. Rodent-borne zoonotic parasites and antibodies to the parasites reported in
Bacteria names Reporting hosts References
Qatar.
Parasite name Reporting hosts References
Acinetobacter baumannii Human and Rodent [18,21]
Aeromonas salmonicida Rodent [18] Helminths
Campylobacter jejuni Chicken, camel, cattle, sheep, [22–24] Echinococcus granulosus Humans, sheep, and [59]
Human, Animal product and farm goats
Campylobacter coli Chicken, camel, cattle, sheep, [22–24] Hymenolepis diminuta Rodents [19,22]
Human, Animal product and farm Hymenolepis nana Humans [60,61]
Campylobacter laridis Human [24] Schistosoma mansoni Humans [62,63]
Campylobacter upsaliensis Human [24] Taenia spp. Humans [61,64]
Corynebacterium sp. Central fresh product market [25] Taenia taeniaeformis Cats and rodents [19,65,66]
Citrobacter freundii Rodent, Human [18,26] Toxascaris leonina Cats [65,67]
Citrobacter koseri Rodent, Human [18,26] Trichuris trichiura Humans [68,69]
Coxiella burnetii Human [27]
Enterobacter aerogenes Rodent, Human [18,26]
Enterobacter cloacae Rodent, Human [18,26] Protozoa
Escherichia coli Human, camel, cattle, chicken, and [18,25,28–37] Cats, dogs, and
Babesia spp. [45,70]
sheep, rodent, and environmental humans
samples Cryptosporidium spp. (C, parvum, C. hominis,
Humans [71,72]
Hafnia alvei Rodent [18] C. meleagridis)
Klebsiella pneumoniae Rodent, Human [18,26] Entamoeba spp. (E. hominis, E. disper) Humans [61,71,73]
Listeria monocytogenes Human [38] Giardia spp. (G. duodenalis) Humans and rodents [19,61,73]
Providencia stuartii Rodent [18] Cats, dogs, and
Leishmania spp. [19,74]
Proteus mirabilis Rodent [18] rodents
Pseudomonas aeruginosa Rodent, Human [18,26] Cat, rodents, and
Toxoplasma gondii [19,75–78]
Mycobacterium tuberculosis Human [39–43] humans
Rickettsia spp. Rodents, dogs, and cats [18,44,45] Trypanosoma lewisi Rodents [19]
Salmonella spp. (including Animal holding, human, livestock [18,24,46–52]
Salmonella enterica) (camel and cattle), and rodents
Yersinia spp. Human [34]
Table 4
Public health importance vectors reported in Qatar that can intervene rodent-
borne zoonoses transmission.
Table 2 Vector Reported Potential role for pathogen References
Rodent-borne zoonotic viruses and viral antibodies reported in Qatar. hosts transmission
Pathogen name Reporting hosts References Sand fly
Chikungunya virus Human [53] Phlebotomus – Leishmania spp. [79,80]
Hepatitis E virus Human [54,55] papatasi
Rabies virus Human, camel, and fox [56]
West Nile Disease virus Human, horse [57,58] Flea
Xenopsylla astia Rodent Yersinia pesits, Rickettsia spp., [14,80]
Hymenolepis diminuta
seroconversion to WNV-pE-Ab were detected in horses of Qatar [58]. Xenopsylla Rodent Yersinia pestis, Hymenolepis [79–84]
cheopis diminuta, Rickettsia spp.,
3.1.3. Parasitic pathogens Bartonella spp.
Ctenocephalides Cat Bartonella spp. Rickettsia spp. [79,80]
Several rodent-borne parasites were reported in humans and animals
felis
of Qatar (Table 3). Hymenolepis diminuta has been reported to be a highly
prevalent helminth in rodents in this country. Whereas H. nana was
Mite
found only in humans. Toxoplasma gondii is prevalent in humans, ro Ornithynyssus Rodent Coxiella burnetii, Rickettsia spp. [19,81,82]
dents, and cats. Leishmania spp. was found in dogs and cats. bacoti
Ticks
3.2. Factors associated with rodent-borne pathogens Hyalomm Camels, Crimean-Congo hemorrhagic [79,80]
dromedarii cattle fever virus, Rickettsia spp.,
During the review of the literature and the field investigation, we Coxiella burnetii
identified several factors, which can be associated with rodent-borne Hyaloma Camels, Crimean-Congo hemorrhagic [79,80]
impeltatum cattle, sheep fever virus, Rickettsia spp.
pathogen emergence in Qatar.
Mosquito
3.2.1. Vectors
Aedes aegypti Humans Chikungunya virus [79,80]
Many vectors, which can facilitate in transmission of several bacte Culex pipiens Human West Nile Virus [79,85,86]
rial, viral, and parasitic diseases were found in Qatar (Table 4). Orni Culex univittatus Mammals West Nile Virus [79,80]
thonyssus bacoti and Xenopsylla astia, which can be the vectors of
Rickettsia spp. were reported in rodents. In addition, several other vec
tors, such as sand fly, ticks, mosquito vectors are available in this rodents. These pest control service providers work based on their indi
country. vidual strategies. The service beneficiaries are mostly corporate offices,
industries, residential areas, major public parks, and other public places.
3.2.2. Rodent control services However, limited interventions are applied in livestock and agricultural
There are no clear rodent control guidelines in Qatar. Ministry of farms.
Municipality of Qatar has pest control unit, which provide public service
in pest control to the citizens and residents. There are several corporate 3.2.3. Drivers of rodent-borne zoonoses
services which manage pest control within the country, including Based on the changes over the past 70 years in Qatar, some of the
3
Md.M. Islam et al. One Health 16 (2023) 100517
following drivers could influence rodent population and rodent-borne other areas [17]. Due to the close proximity between humans and
disease emergence in Qatar: (1) oil and gas revolution, (2) rapid in multispecies animals with poor biosecurity management in the Qatari
crease of multicultural population, (3) rapid urbanization, (4) impor livestock farms, there is the chance of species jumping of zoonotic
tation of food and agricultural products, (5) agricultural and livestock pathogens at human and animal interface, observed in MERS-CoV cases.
development, (6) farm biosecurity, and (7) stray animals. The owner, worker, and camels of the same farm were found positive for
In the past, Qatar was inhabited primarily by Bedouins who mainly MERS-CoV [87]. Although there is no documented report of stray dogs
delved in fishing, pearl harvesting, and livestock farming. Ever since the and cats in Qatar, according to the newspaper reports [104–106], there
oil revolution in the 1950s, economic development and globalization is a rise in the numbers of stray cats and dogs in this country, which can
[87–89] has attracted high numbers of skilled, semi-skilled, and un- influence the transmission cycle of the rodent-borne pathogens [5].
skilled workers [88,90] (Fig. 1). This migration played an important
role in determining population change and a dynamic socio-economic 3.2.4. Possible transmission dynamics
environment in this country. In 1960s, Qatar’s population was only Rodent-borne pathogens can be transmitted to humans by direct
47,000, by the 21st century it had increased 12 folds [91], with over 2.7 contact from rodents, however, they can also be mediated through inter
million in 2020 with considerable industrial and commercial develop and intra-species transmission among vectors or reservoirs, such as
ment [92]. This change could disrupt the rodent ecosystem in the de livestock, pets, and arthropods (Fig. 5). Certain diseases can be imported
serts, forcing them to migrate toward the cities. Generally, rodents tend to Qatar by the immigrant workforce, pets, and food and agricultural
to live within city limits due to vast availability of food resources and product importation, such as Leishmaniasis, Salmonellosis, Mpox, and
less risk of predation [93]. Rabies (Fig. 6). Many partner countries, such as Bangladesh, India,
As a desert country, Qatar initially had minimal agricultural activ Nepal, Sri Lanka, Iran, Pakistan, and Egypt from where major immigrant
ities but that has changed in the last decade [94,95]. The country im work force, food and agricultural products imported are endemic with
ports food and agricultural products from different countries. The rodent-borne zoonotic diseases, such as, Hymenolepis nana, Hepatitis E,
annual cost of food import rose from around $100 million in 2000 to Enteric fever, Leishmaniasis, and Schistosomiasis [51,52,107–110].
$1000 million in 2018 [96] (Fig. 2). Some major partner countries for Most of these diseases were reported among the immigrant residents in
importation of manpower, live animal and food products include: India, Qatar, especially among the newly immigrant residents, which indicates
Bangladesh, Nepal, Sri Lanka, Pakistan, Philippines, Egypt, Turkey, and that such diseases were imported to Qatar by the immigrant workforce,
Sudan [96,97]. These countries are endemic with many rodent-related such as Giardiasis and Cryptosporidiasis [61,73,111].
diseases, such as rabies, typhoid fever, chikungunya, leishmaniasis,
and Rift Valley fever [98–102]. As such, any kind of trade or travel from
3.3. Expert opinion
these countries presents a risk of various diseases being imported within
Qatar [5].
The species diversity, population density and distribution, and pop
There has been an increase in agricultural practices in recent years in
ulation burden of rodents in Qatar is still unknown. Which is why it is
Qatar. The amount of vegetated area and arable land increased from
essential to conduct scientific investigations to estimate actual rodent
5.3% to 5.8%, and 6.8% to 7.2%, respectively from 1999 to 2018 [96]
population density and geographic distribution, especially to identify
(Fig. 3). Since the blockade in Qatar in 2017, the local food production
abnormal population diversity, habitats, and ecology. The experts’
has increased, and several animal and vegetable farms started operating
opinion emphasized that mixed species animal farming, inadequate
locally to distribute food in the market for human consumption. The
biosecurity measures, and poor animal housing and agricultural prac
number of livestock and livestock farms has also been increased by 3
tices in farms tend to increase the risk of zoonoses. Urine and feces from
times in the last 10 years [103] (Fig. 4). In Qatar, livestock farms are
rodents can contaminate animal feed, which can eventually lead to
mainly managed traditionally with insufficient biosecurity measures.
transmission among animal handlers, especially if there is a lack of
These farms are generally keeping mixed livestock, captive wild ani
biosafety and biosecurity measures implemented on the farms. Devel
mals, exotic birds, and pets within a single boundary (usually within 50
opment and implementation of appropriate legislation and guidelines
× 50 square meter space). The majority of farmworkers are from
can be used to mitigate such risks and ensure placement of biosafety and
Bangladesh, India, Nepal, and Sudan and live in the farm compound.
biosecurity.
The owners keep their resting place (majlis) inside the farm where they
Rapid urbanization and global climate change together can alter the
spend their evening and holiday times. Our study demonstrates that
ecosystem of a country and directly impact proliferation of vectors and
livestock and agricultural farms are more prevalent with rodents than
vector-borne diseases (VBDs), especially with regards to change in
Fig. 1. Qatar population growth from 2000 to 2019 (left) and population distribution by country of origin in 2019 (right) [91,92,97].
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Md.M. Islam et al. One Health 16 (2023) 100517
Fig. 2. Food and agricultural product import in Qatar from 2000 to 2018 (left) and the partner countries to import in 2018 (right) [96,97].
Fig. 3. Changes in land use for agricultural and arable purpose from 1999 to 2018 in Qatar [96].
Fig. 4. Changes in number of total livestock and livestock farms from 2012 to 2020 (left) and distribution of livestock animals in 2020 (right) [103].
pathogen characteristics, host diversity, transmission, and distribution, of emergence for Schistosomiasis with immigrant workers, while some
finally emergence of novel pathogens. It was highly emphasized that others mentioned the risk of a pathogen being imported by immigrant
vectors need to be investigated to check for the presence of pathogens to workers is minimal, even via food imports. Overall, they all agreed that
mitigate any possible threat of VBDs as early as possible. It was risk of imported pathogen should not be omitted without proper
mentioned that dogs and falcons should also studied since they are used investigation. Consensus between the experts was to conduct a risk
in sporting activities and can possibly contract VBDs, then transmit them assessment of rodent-borne zoonoses to gauge existing gaps and mitigate
through contact with infected rodents. By extension, stray cats too these risks. Additionally, seaports and airports should be focus of
should be kept in check in order to avoid spread of VBDs. Some experts stronger surveillance practices to minimize risks of rodent-borne zoo
cited Oman, a member country of the Arabian Peninsula, as an example noses in Qatar. Regarding food chain, experts think that it is essential to
5
Md.M. Islam et al. One Health 16 (2023) 100517
4. Discussion
Fig. 6. The global map showing the top 15 partner countries for manpower, food, and agricultural product importation. Transboundary transmission of such diseases
can happen to Qatar from these partner countries.
6
Md.M. Islam et al. One Health 16 (2023) 100517
7
Md.M. Islam et al. One Health 16 (2023) 100517
Fig. 7. Evidence based One Health investigation to prevent rodent-borne zoonoses. Rodent infestation reports will be provided to the One Health team. The One
Health team will collect the records of vectors and hospitals and analyze with rodent infestation. Then after joining the local community, policy makers, media and
lobby groups, a unified decision will be taken and applied to investigate and prevent rodent-borne zoonoses in Qatar.
lobbyists, educate the citizens and residents, and essentially develop residential complexes, business centers, airport, and seaports in Qatar.
collective consciousness. Different facilities require different length of control strategies to be put
Although animal ethics are closely practiced for animals used in in place, such as short-medium-long. A short-term solution addresses the
experiments, however, these principles are not followed for when immediate rodent control problem, whereas a long-term plan focuses on
certain animals are considered pests. Despite being regarded as pests, understanding rodent ecology and risk factors. In the residential,
rodents deserve to be handled with humane considerations. Hence, an corporate, and industrial areas, short-term or emergency rodent control
Integrated Pest Management (IPM) program can be amended within the is applicable. Higher emphasis should be given to the livestock and
rodent control program to ensure ethical measures are followed in agricultural areas. Development and application of biosecurity measures
management of rodents across Qatar [118]. A national IPM guideline in livestock and agricultural farms is vital in control of rodents and
can be developed, in which local facilities, ecosystem interaction be rodent-borne zoonoses. This can be achieved via support from legisla
tween humans, livestock, pets, and rodents, socio-economic balance, tion and law enforcement, which will not only help reduce rodent in
local culture, and cost-benefit will be respected. IPM can serve as a festations, but also decrease prevalence of zoonotic diseases of concern.
quality check for biosafety and management procedures in the hospitals,
8
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