Epidemiology and Infection Outbreak of highly pathogenic avian influenza
in Ghana, 2015: degree of losses and outcomes
cambridge.org/hyg
of time-course outbreak management
1
Original Paper W. Tasiame , S. Johnson
2, V. Burimuah1, E. Akyereko3, P. El-Duah4, E. Amemor1,
B. O. Emikpe1 and E. W. Owiredu5
Cite this article: Tasiame W, Johnson S,
Burimuah V, Akyereko E, El-Duah P, Amemor E, 1School of Veterinary Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, PMB, UPO,
Emikpe BO, Owiredu EW (2020). Outbreak of 2
highly pathogenic avian influenza in Ghana, Kumasi 00233, Ghana; School of Veterinary Medicine, CBAS, University of Ghana, Legon, Accra, Ghana;
3Disease
2015: degree of losses and outcomes of time- Surveillance Department, Ghana Health Service, Accra, Ghana;
4Kumasi Centre for Collaborative Research in
course outbreak management. Epidemiology Tropical Medicine, PMB, UPO, Kumasi 00233, Ghana and
5Department of Molecular Medicine, School of Medicine
and Infection 148, e45, 1–8. https://doi.org/ and Dentistry, Kwame Nkrumah University of Science and Technology, PMB, UPO, Kumasi 00233, Ghana
10.1017/S095026882000045X
Abstract
Received: 29 October 2019
Revised: 5 January 2020 This retrospective study highlights the degree of losses and time-course through which the
Accepted: 11 February 2020 2015 highly pathogenic avian influenza (HPAI) outbreaks in Ghana were managed. A total
Key words: of 102 760 birds from 35 farms across five regions in Ghana included in this study were
HPAI; management; outbreak; time-course affected. Out of this, 89.3% was from the Greater Accra region. Majority of the birds were
culled (94.2%). Adult layers were most affected and destroyed (64.0%), followed by broilers
Author for correspondence: (13.7%). Event initiation to reporting averaged 7.7 ± 1.3 days (range: 1–30 days). Laboratory
E. W. Owiredu, confirmation to depopulation of birds averaged 2.2 ± 0.5 (0–15) days while depopulation to
E-mail: eddiewilliams.owiredu@gmail.com
disinfection took 2.2 ± 0.7 (0–20) days. Overall, some farms took as long as 30 days to report
the outbreak to the authorities, 15 days from confirmation to depopulation and 20 days from
depopulation to disinfection. On average, outbreak management lasted 12.3 (2–43) days from
event initiation to depopulation. The study reveals a significant number of avian losses and
delays in HPAI reporting and management by the authorities in Ghana during the 2015 out-
break. This poses a high risk of spread to other farms and a threat to public health. Awareness
creation for poultry farmers is necessary for early reporting, while further study is required to
set thresholds for the management of such outbreaks by veterinary departments.
Introduction
Avian influenza (AI) is an epidemic viral infection caused by avian influenza Type A viruses [1].
There are two distinct types of influenza A viruses that infect poultry based on their disease-
causing capabilities. Whereas the highly pathogenic avian influenza (HPAI) causes severe illness
in domestic birds with high mortalities, the low pathogenic avian influenza (LPAI) manifests
milder symptoms [2]. Direct contact with infected and dead birds is probably the most reported
mode of transmission to humans [3]. Apart from its public health significance, AI exerts an
enormous toll on the socio-economic status of countries during outbreaks [4].
Historically, the major spread of HPAI H5N1 virus began in eastern and southeastern Asia
from 2003 through 2004. In 2005–2006, HPAI had moved westward across Asia into Europe,
the Middle East and Africa [5]. The AI epidemic in Asia resulted in the infection of all species
of domestic poultry within 8 years (1997–2005) [6]. In Africa, HPAI was first reported in
Nigeria in 2006 [7]. This was also the first reported outbreak of the H5N1 Asian strain on
the African continent. Egypt was the second African country to be infected with H5N1.
Over 30 million birds were reportedly culled; an estimated 250 000 jobs and a high number
of human lives were lost as a result [8]. The Food and Agriculture Organization (FAO) of
the United Nations (UN) also reported HPAI H5N1 outbreaks in Togo and 10 other
African countries from February 2006 to July 2008 [9].
© The Author(s), 2020. Published by In Sub-Saharan Africa, countries endemic with HPAI H5N1 include Burkina Faso,
Cambridge University Press. This is an Open Cameroon, Côte d’Ivoire, Niger, Nigeria, Togo and Ghana [10]. It is believed that the out-
Access article, distributed under the terms of breaks of AI in neighbouring countries may have influenced the outbreaks in Ghana. After
the Creative Commons Attribution licence
(http://creativecommons.org/licenses/by/4.0/), the first outbreak of HPAI and its management in Ghana, several programmes were carried
which permits unrestricted re-use, out to educate the public on biosecurity measures. Active AI surveillance was conducted on
distribution, and reproduction in any medium, different types of birds using real-time polymerase chain reaction (PCR) with no positive
provided the original work is properly cited. case for influenza A [8]. Ghana did not report any further outbreaks of HPAI since the
2006–2007 wave until Nigeria recommenced reporting positive cases in January 2015 [11].
The primary administrative regions in Ghana affected were Greater Accra, Ashanti, Central,
Eastern, Volta and Western region, and a total of 63 outbreaks have been reported as of
November 2016 [10]. Though the provenance of HPAI H5N1 in Ghana has not been explicitly
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https://doi.org/10.1017/S095026882000045X
2 W. Tasiame et al.
Fig. 1. Map showing the 2015 HPAI outbreaks sites and the time of outbreaks. The numbers represent the time-lines for each outbreak (numbers do not add up
because some outbreaks were too close and thus overlapped).
outlined, a report by Mabbett indicates a 98.8–99.6% homology spans a landmass of 238 535 km2, and it is bordered by Ivory
with isolates from Burkina Faso, Cote d’Ivoire, Nigeria and Coast to the west, Burkina Faso to the north, Togo to the east
Sudan [12]. and the Gulf of Guinea and the Atlantic Ocean to the south. It
The detrimental effects of HPAI on the poultry industry as lies on the latitude 7.9528 and the longitude −1.0307 [18].
well as its threat to public health necessitated the establishment Study sites included were the Ashanti, Central, Volta, Western
of Technical Committee of Experts on Prevention and Control and Greater Accra regions, which constitute five of the total 10
of Avian Influenza tasked with developing strategies for the pre- administrative regions of Ghana. A total of 35 farms across the
vention of the disease, surveillance networks and emergency pre- five regions were included in the study. Areas captured were
paredness plans for disease containment [13, 14]. Nonetheless, those who reported AI outbreaks within the study period. All out-
insufficient financial and logistical resources, weak Veterinary break sites and the time-line for each outbreak were
Services, lax border controls on animal movements, conflicts geo-referenced (Fig. 1).
and inappropriate governance provide an enabling environment Data for this study were obtained from the epidemiology unit
for the spread of HPAI and other transboundary animal diseases of the Veterinary Services Department under the Ministry of Food
[15]. This is evidenced in the recent confirmation of AI virus sub- and Agriculture, Ghana. Checks were made from the affected
type H9N2 in 2018 [16]. region and district veterinary offices for confirmation before use
The poultry industry in Ghana remains at its juvenile stage. for this review. The retrieved data consist of AI outbreaks from
There is thus a critical need to monitor all health-related circum- January through December of 2015. Data captured included AI
stances that endanger it. HPAI not only infects poultry but also cases from the backyard, small-scale commercial and free-range
the humans who tend for the birds [17]. It is therefore imperative poultry. Other variables assessed included bird population, type
to have sufficient knowledge on the outbreaks of AI that occurred of birds, number of birds destroyed, natural deaths (died prior
in Ghana and the time-course through which these outbreaks to the depopulation events), and dates of initiation of event, con-
were managed. This information would equip policymakers firmation, depopulation and disinfection. Districts and regions
with the necessary information to develop apt strategies to affected in these outbreaks were also captured. Avian species cov-
improve upon the management of future outbreaks. It is against ered included chickens, ducks, pigeons, turkeys and guinea fowls.
this background that this study analysed the 2015 AI outbreak Approval for this study was obtained from the National
data in Ghana to evaluate the degree of losses and time-course Epidemiology Unit of Veterinary Services of Ghana, the source
of its management. that generated these data.
Methods
Statistical analysis
Study area and outbreak data
Statistical analysis was performed using the R Language for
The study was a retrospective analysis of AI outbreak data from Statistical Computing version 3.6.0 [19]. Categorical and continu-
Ghana in 2015. Ghana is located along the Gulf of Guinea and ous data were expressed as frequencies (percentages) and means
the Atlantic Ocean, in the sub-region of West Africa. Ghana ± standard error of the mean, respectively. Independent t test and
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https://doi.org/10.1017/S095026882000045X
Epidemiology and Infection 3
Table 1. Distribution of avian losses by avian influenza affected regions in Ghana, 2015
Region No of farms affected Bird population Bird destroyed Natural deaths Eggs destroyed (crates)
Ashanti 1 1948 (1.9) 1883 (96.7) 65 (3.3) 12 (0.7)
Central 1 510 (0.5) 476 (93.3) 34 (6.7) 4 (0.2)
Volta 2 3400 (3.3) 950 (27.9) 2450 (72.1) 18 (1.1)
Western 2 5131 (5.0) 3459 (67.4) 1672 (32.6) 2 (0.1)
Greater Accra 29 91 771 (89.3) 70 016 (76.3) 21 755 (23.7) 1628 (97.8)
Total 35 102 760 (100) 96 784 (94.2) 25 976 (25.3) 1664 (100)
Percentages for bird population and number of eggs destroyed were calculated by column. Percentages for birds destroyed and natural deaths were by rows, using bird population as the
denominator.
one-way ANOVA were used to determine the significance of dif- To evaluate the influence of farm size – defined as the number
ferences between farm sizes, farm types and administrative zones of poultry on each farm – and farm type on the time-course of the
in relation to time-course management, respectively. A P-value management, we grouped farms into those having <1000 and
<0.05 was considered statistically significant. ≥1000 birds and commercial, backyard and free-range, respect-
ively. Farms with ≥1000 birds consistently presented with higher
duration for management across all events; however, only the
Results time-course from confirmation to depopulation was statistically
Overall, 102 760 birds originating from 35 farms across five major significant (1.2 ± 0.3 vs. 3.2 ± 0.8 days, P = 0.034). No statistically
regions were included in the study. Out of this figure, the Greater significant differences were observed for farm type (Fig. 4).
Accra region recorded the highest proportion (89.3% (91771/
102760)) and the remainder was distributed among the other
Discussion
four regions. A total of 5976/102760 (25.3%) of the birds affected
died naturally as a result of HPAI (prior to the depopulation In 2015, Ghana experienced HPAI outbreaks which began in
events), with the Volta region recording the highest number of April and ended in December, with peak outbreaks in June–
natural losses (2450/3400 (72.1%)). On the other hand, the July. The outbreak has been proposed to have originated from
Ashanti region recorded the highest proportion of avian losses Nigeria. Sequence analysis of the viral hemagglutinin revealed
by culling (1883/96784 (96.7%)). Approximately 98% (1628/ that the 2015 Ghana outbreak strain possessed a multi-basic
1664) of the eggs destroyed originated from Greater Accra cleavage site (RERRRKR/GLF), as common to HPAI H5N1
(Table 1). viruses [20]. Phylogenetic analysis confirmed that the strain
The outbreak began in April 2015 with three incidents that belonged to clade 2.3.2.1c. Genetic analysis of polymerase basic
continued spreading throughout the year. Cases peaked in June protein 2 showed that the strain lacked the known human adap-
through July before recording a downward trend in subsequent tive signatures E627K or D701N [11]. Nucleoprotein sequences of
months (Fig. 2a). Most of the farms affected were small-scale isolates from Ghana revealed 99% homology with the Nigeria
commercial farms (51.4% (18/35)) (Fig. 2b) and adult layers 2015 outbreak strain, confirming the high probability of the origin
were the most affected and destroyed (61942/96784 (64.0%)). of the virus [11]. Small-scale commercial farms were the most
Available dressed chickens ready for market were also destroyed affected and a total of 102 760 bird losses were incurred. The
(775/96784 (0.8%)) (Fig. 2c). Additionally, out of the 6.0% losses losses were predominantly in the Greater Accra region. This
for birds other than domestic fowls, ducks recorded the greatest was expected because 29 out of the 35 farms affected were located
loss (4012/5807 (69.1%)) (Fig. 2d). in the region. The region is also home to the international airport
The average duration from the initiation of the event to report- and main seaport which could have facilitated free and increased
ing was 7.7 ± 1.3 (range: 1–30) days while that from reporting to the inflow of persons and goods, enabling increased chance of
laboratory confirmation was 2.7 ± 0.5 (0–13) days. The duration spreading. Undoubtedly, the increased number of affected birds
from laboratory confirmation to depopulation of birds was 2.2 in the Greater Accra region may also be attributed to the proxim-
± 0.5 (0–15) days and depopulation to disinfection lasted for ity of farms within the region. Congruently, Saidu et al. [1]
2.2 ± 0.7 (0–20) days. Overall, it took as long as 30 days to report observed that the proximity of farms during outbreaks facilitated
the outbreak after initiation of the event for some farms, 15 days rapid spreading. Turkson also reported that the free flow of goods,
from confirmation to depopulation and 20 days from depopula- people, poultry and poultry products, through approved and
tion to disinfection. Additionally, for some cases, it took unapproved borders, is a major means of introducing diseases
13 days for laboratory confirmation after reporting (Fig. 3a). such as HPAI into Ghana [21]. Furthermore, trading of live
Taken together, the average duration from event initiation to birds once a possible outbreak is announced may be partly
depopulation was 12.3 ± 1.7 (2–43) days whereas from event ini- involved. Morris et al. [22] indicated that, in countries where dis-
tiation to disinfection was 14.6 ± 2.0 (2–47) days (Fig. 3b). ease outbreaks are poorly controlled, farmers usually respond to
Strikingly, upon stratification by administrative zones, Western the situation by selling their birds to reduce their financial losses.
region, despite presenting with only two outbreak cases, recorded This attitude may have also facilitated the spread of the disease
the highest mean duration from event initiation to depopulation, from the source of the outbreak in Accra, within the region and
although not statistically significant (P-value >0.05 for all com- to neighbouring regions such as the Volta region which shares
parison) (Fig. 3c and 3d, Supplementary Table S1). a border with Greater Accra, with several entry points for the
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4 W. Tasiame et al.
Fig. 2. Epicurve of outbreaks and descriptive statistics of the type of farm and birds affected. (a) Epicurve showing the number of outbreaks per month.
(b) Distribution of the type of farm affected. (c) Avian influenza losses by the type of bird (percentages were calculated using the total number of birds destroyed).
(d) Avian influenza losses for birds other than domestic fowl (percentages were calculated using the total number of birds destroyed other than domestic fowl).
movement of good and people. Outbreaks in other regions are contacts [27]. Thus, small-scale poultry farms that rear birds
likely to be due to the poorly-regulated trans-regional trade of other than domestic fowls also contribute to the transmission
live birds, a fairly common practice by poultry farmers in the of AI. It should, however, be noted that since Newcastle disease
country. was not assessed, the significance of pigeons in this study may
The predominant species of birds affected were domestic be limited.
chickens, followed by ducks, pigeons, turkeys and guinea fowls. The strength of this study is in reporting the time-course of
Among the chickens, adult layers were the most affected and management during the 2015 AI outbreak in the country. The
destroyed. This finding is in harmony with the findings of first case of HPAI H5N1 among poultry in Ghana was reported
Saidu et al. [1] and Akanbi et al. [23] in Nigeria who reported in 2007 [11, 28]. The outbreak occurred in three regions:
a similar trend. The FAO indicated that domestic fowl, ducks, Greater Accra, Volta and Brong Ahafo. After containing the
geese, turkeys, guinea fowl, quail and pheasants are all susceptible 2007 HPAI H5N1 outbreak, active AI surveillance was initiated.
to AI, although outbreaks predominantly occur in domestic fowl Due to the high losses during the 2007 outbreak, it was expected
and turkeys [24]. Other studies have also reported that other that the influenza surveillance will consider the limitations and
avian species such as ducks, turkeys, geese, etc., play vital roles build on the past experiences for a more resilient and timely
in the epidemiology of AI [23, 25, 26]. Moreover, ducks have approach towards new outbreaks. However, we observed consid-
been implicated in the transmission of LPAI and HPAI virus erable delays from the onset of clinical signs through the confirm-
among themselves and other domestic birds via direct or indirect ation of disease to the initiation of control measures during the
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https://doi.org/10.1017/S095026882000045X
Epidemiology and Infection 5
Fig. 3. Time-course management of HPAI outbreak. (a, b) Time-course from event initiation to disinfection across all outbreak sites. (c, d) Time-course from event
initiation to disinfection stratified by administrative zones.
2015 HPAI H5N1 outbreak. Timely reporting and confirmation within a day of onset of clinical signs and the disease was success-
are key to control the spread of the disease. Delays in these events fully eradicated within three-and-a-half months, following an
affect downstream measures such as the times for destruction of eradication campaign. This underscores the significance of early
all birds on affected farms, disinfection of affected farms and reporting and confirmation in the control of AI and could be
restricted movement of poultry and poultry products. Of note, the major reason why the outbreak in Ghana took over 9 months
there were also delays from confirmation to depopulation and for complete containment to be achieved. We attribute the delay
subsequent disinfection which may have aggravated the rapid dis- in reporting partly to a lack of knowledge of the disease among
semination of the disease across regional borders. In 2004, Japan farmers. Education of farmers regarding AI, its pathology, control
reported HPAI H5N1 cases in four different premises [29]. Out of and possible preventive measures will be thus indispensable in the
this, three farms reported the cases to the appropriate authorities stride against AI in Ghana and Africa.
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6 W. Tasiame et al.
Fig. 4. Time-course management of HPAI outbreak by
farm size and farm type. (a, g) Event initiation to reporting.
(b, h) Reporting to confirmation. (c, i) Confirmation to
depopulation. (d, j) Depopulation to disinfection. (e, k)
Event initiation to depopulation. (f, l) Event initiation to
disinfection.
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Epidemiology and Infection 7
In Ghana, before the transportation of suspected HPAI sam- Acknowledgments. The authors express their gratitude to all the staff of the
ples to the International Reference Laboratory for Newcastle National Epidemiology Unit of Veterinary Services of Ghana for providing the
Disease and Avian Influenza, Italy, for confirmation, the samples source data for this study.
undergo initial internal screening. The initial diagnosis is done Financial support. This research received no specific grant from any fund-
through rapid tests, conventional PCR and currently, real-time ing agency, commercial or not-for-profit sectors.
PCR. The laboratory is however located only in Accra, the capital
of Ghana. Thus, distance, coupled with unfavourable transporta- Conflict of interest. None.
tion routes, may have also played a role in the delays observed in
this study. Inadequate supply of consumables such as laboratory
reagents and bureaucratic delays has also been identified as a
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