Received: 3 January 2020 | Revised: 2 March 2020 | Accepted: 2 March 2020

DOI: 10.1111/jfd.13164

REVIEW

The nature and consequences of co-infections in tilapia:

A review

Hany M. R. Abdel-Latif1 | Mahmoud A. O. Dawood2 |

Simon Menanteau-Ledouble3 | Mansour El-Matbouli3

1
Department of Poultry and Fish diseases,
Faculty of Veterinary Medicine, Alexandria
University, Alexandria, Egypt
2
Department of Animal Production, Faculty
of Agriculture, Kafrelsheikh University,
Kafrelsheikh, Egypt
3
Clinical Division of Fish Medicine,
University of Veterinary Medicine Vienna,
Vienna, Austria
Correspondence
Hany M. R. Abdel-Latif, Department of
Poultry and Fish Diseases, Faculty of
Veterinary Medicine, Alexandria University,
Edfina 22758, Egypt.
Emails: hmhany@alexu.edu.eg;
healthyfish.20@gmail.com
Abstract
Co-infections commonly arise when two or multiple different pathogens infect the
same host, either as simultaneous or as secondary concurrent infection. This po-
tentiates their pathogenic effects and leads to serious negative consequences on
the exposed host. Numerous studies on the occurrence of the bacterial, parasitic,
fungal and viral co-infections were conducted in various tilapia species. Co-infections
have been associated with serious negative impacts on susceptible fish because they
increase the fish susceptibility to diseases and the likelihood of outbreaks in the af-
fected fish. Co-infections can alter the disease course and increase the severity of
disease through synergistic and, more rarely, antagonistic interactions. In this review,
reports on the synergistic co-infections and their impacts on the affected tilapia spe-
cies are highlighted. Additionally, their pathogenic mechanisms are briefly discussed.
Tilapia producers should be aware of the possible occurrence of co-infections and
their effects on the affected tilapia species and in particular of the clinical signs and
course of the disease. To date, there is still limited information regarding the patho-
genicity mechanisms and pathogen interactions during these co-infections. This is
generally due to low awareness regarding co-infections, and in many cases, a domi-
nant pathogen is perceived to be of vital importance and hence becomes the target
of treatment while the treatment of the co-infectious agents is neglected. This re-
view article aimed at raising awareness regarding co-infections and helping research-
ers and fish health specialists pay greater attention to these natural cases, leading
to increased research and more consistent diagnosis of co-infectious outbreaks in
order to improve control strategies to protect tilapia when infected with multiple
pathogens.

KEYWORDS

co-infections, susceptibility, synergistic interactions, tilapia

1 | I NTRO D U C TI O N
Aquaculture is the fastest-growing food production sector, and it is
considered a central part of ensuring food safety in the developing
world (FAO, 2017). Among the varied fish species farmed, tilapia is the
second most important in volume after cyprinid fish, and this species
is farmed in over 100 countries worldwide (FAO, 2017), especially in
China (1.8 MT), Indonesia (1.1 MT) and Egypt (875 thousand tonnes)
(FAO, 2017). The worldwide production of tilapia was estimated to be
4.5 MT in 2014, and it is expected to rise to 7.3 MT in 2030 (FAO, 2014).

J Fish Dis. 2020;00:1–14. wileyonlinelibrary.com/journal/jfd© 2020 John Wiley & Sons Ltd | 1
2 |
The term “tilapia” is a common usage term that refers to multiple
species belonging to several fish genus, most notably Oreochromis
and Sarotherodon. Among the characteristics that explain the pop-
ularity of this species are its adaptability, resistance to many dis-
eases and suitability for culture under intensive farming conditions
(FISHSTAT, 2015).
Despite the robustness of tilapia, outbreaks of diseases, particu-
larly of bacterial origin, remain one of the main limiting factors that
threaten tilapia production, specifically when cultured under inten-
sive conditions (El-Sayed, 2019). Fish diseases often occur following
an initial stressor, and in the case of infectious disease, it is common
that more than one pathogen can be identified (Kotob, Menanteau-
Ledouble, Kumar, Abdelzaher, & El-Matbouli, 2017; Mustafa, Speare,
Daley, Conboy, & Burka, 2000; Roon, Alexander, Jacobson, &
Bartholomew, 2015; Zhang, Li, Chi, Ling, & Wang, 2015).
Co-infections are defined by the concurrent presence of more
than one pathogen (Cox, 2011). Interactions between the invading
pathogens often drastically alter the host susceptibility to infec-
tion, disease course, severity and duration of the infection (Graham,
Cattadori, Lloyd-Smith, Ferrari, & Bjornstad, 2007; Telfer et al.,
2008), and are synergistic, resulting in elevated pathogenicity of
one or both pathogens. However, antagonistic interactions have also
been described, resulting in the suppression of one or both of the
pathogens (Bradley & Jackson, 2008).
Several instances of natural concurrent infections with differ-
ent pathogens have already been reported in various tilapia spe-
cies (Amal et al., 2018; Cutuli et al., 2015; Dong et al., 2015; Eissa,
Tharwat, & Zaki, 2013; Eissa, Zaki, & Aziz, 2010; Nicholson et al.,
2017; Nicholson, Mon-on, Jaemwimol, Tattiyapong, & Surachetpong,
2019; Nofal & Abdel-Latif, 2017; Ramírez-Paredes et al., 2019). In
addition, numerous dual-infection studies have been conducted in
order to evaluate the link between the two co-infecting pathogens
under laboratory conditions (Xu, Shoemaker, & Klesius, 2007, 2009;
Xu, Shoemaker, & LaFrentz, 2014; Xu, Shoemaker, & Zhang, 2015).
These reports and studies have shown significant differences
both in terms of pathogenic mechanisms, disease course and sever-
ity of the infection and in terms of the clinicopathological feature
between co-infections and the pathogens in isolation. In this con-
text, it is important to collate and summarize the numerous reports
and studies on co-infections in tilapia species and assess the effects
of these interactions.
2 | TH E CO - I N FEC TI O N S I N TI L A PI A :
T Y PE S A N D E FFEC T S
The numerous instances of co-infections can be broadly classified
between outbreaks caused by two homologous pathogens of the
same type, such as two bacteria (Table 1), or two or more pathogens
of different types, such as the co-occurrence of a bacterium and a
virus (Table 2). Another distinction is the effect of this co-presence
on the virulence of the pathogens. In most of the reported cases,
the pathogenic agents interacted synergistically with each other,
ABDEL-LATIF et al.
leading to an increase in the disease and mortalities. However, in a
few cases, the opposite has been reported with the co-infections,
leading to an attenuated disease compared with infection with a sin-
gle pathogen (Kotob et al., 2017).
2.1 | Bacterial co-infections
Cultured tilapia are susceptible to several bacterial diseases, such as
francisellosis, caused by Francisella noatunensis subsp. orientalis (Fno)
(Lin et al., 2016; Nguyen, Dong, Senapin, Pirarat, & Rodkhum, 2015;
Soto, Hawke, Fernandez, & Morales, 2009); streptococcosis, caused
by Streptococcus agalactiae (Kayansamruaj, Pirarat, Katagiri, Hirono,
& Rodkhum, 2014; Suanyuk, Kong, Ko, Gilbert, & Supamattaya,
2008), S. iniae (Anshary, Kurniawan, Sriwulan, Ramli, & Baxa, 2014)
and S. dysagalactiae (Costa, Leal, Leite, & Fig ueirdo, 2014); ed-
wardsiellosis, caused by Edwardsiella tarda (Clavijo, Conroy, Conroy,
Santander, & Aponte, 2002) and E. ictaluri (Soto et al., 2012); and
bacterial haemorrhagic septicaemia, caused by several aeromon-
ads including Aeromonas hydrophila (Austin & Austin, 2012), A. so-
bria (Li & Cai, 2011), A. hydrophila subsp. Dhakensis (Soto-Rodriguez,
Cabanillas-Ramos, Alcaraz, Gomez-Gil, & Romalde, 2013) and A. ve-
ronii (Dong et al., 2015; Eissa et al., 2015; Huys, Cnockaert, & Swings,
2005; Nhung et al., 2007).
In Brazil, a survey of the presence of Fno in farm-raised Nile ti-
lapia, Oreochromis niloticus, revealed an instance of natural co-infec-
tions with one fish infected with both S. agalactiae and Fno (Assis,
de Oliveira, Gardner, Figueiredo, & Leal, 2017). The following au-
tumn, an outbreak was reported from cage-reared Nile tilapia and
attributed to co-infections between S. agalactiae and Fno (Assis,
Oliveira, et al., 2017). The diseased fish had suffered from chronic
hypoxia (dissolved oxygen levels in the water below 3 mg/L) prior
to the outbreak, which suggests that the condition might have been
opportunistic. Clinical signs included melanosis, gasping, exophthal-
mia and erratic swimming with significant chronic mortalities (Assis,
Tavares, Tavares, Pereira, Figueiredo, & Leal, 2017). Because of the
likely importance of the stressor in the establishment of the disease,
the role of individual pathogens and their potential synergistic inter-
actions remain unclear. However, experimental co-infections using
both isolates were later successfully induced under laboratory con-
ditions and resulted in an earlier and significantly higher mortality
rate when compared to fish challenged with pure cultures of a single
bacterium.
It has been demonstrated that fish exposure to stressors such
as water temperature, low DO and high stocking densities has a
significant increase in the pathogenicity of the invading pathogens
(Andree, Rodgers, Furones, & Gisbert, 2013; Kayansamruaj et al.,
2014; Mian et al., 2009). Furthermore, it was found that Nile tila-
pia exposed to sublethal levels of DO (<1 mg/L) caused pronounced
higher mortalities due to S. agalactiae infection (Evans, Shoemaker,
& Klesius, 2003). A similar finding was clearly observed in the cage-
and pond-cultured hybrid tilapia (O. niloticus × O. mossambicus) when
exposed to streptococcosis (Amal, Saad, Zahrah, & Zulkafli, 2015).
ABDEL-LATIF et al. | 3

TA B L E 1 Potential co-infections with two or multiple homologous pathogens in tilapia species and their pathogenic effects

Synergistic Study
co-infections Tilapia species The co-infecting pathogens Pathogenic effects area References

Bacterial Cage-farmed Nile tilapia under S. agalactiae and Francisella Immunosuppression Brazil Assis, Tavares, et al.
co-infections chronic hypoxia noatunensis subsp. orientalis and chronic high (2017), Assis, de
mortalities Oliveira, et al.
(2017)
Nile tilapia A. jandaei and A. veronii Disease and significant Thailand Dong et al. (2017)
mortalities
Hybrid red tilapia A. hydrophila and Edwardsiella Pigmentation loss, Malaysia Lee and Wendy,
tarda exophthalmia, eye (2017)
opacity and swelling
at abdomen with a
significant mortality
Red tilapia (Oreochromis sp.) Francisella noatunensis subsp. Vertical transmission Thailand Pradeep et al.
orientalis and Shewanella and concurrent (2017)
putrefaciens infection with these
two bacteria are
evidenced.
Hybrid red tilapia Chronic Francisella noatunensis Rapid and higher rates Thailand Sirimanapong et al.
(O. niloticus × O. mossambicus) with subsequent challenge of mortality. (2018)
with S. agalactiae
Nile tilapia Natural co-infections with Season mortalities Brazil Delphino, Leal, et al.
multiple bacterial pathogens (2019)
such as S. agalactiae, S. iniae,
Francisella noatunensis subsp.
orientalis, A. hydrophila,
Pleisiomonas shigelloides and
Edwardsiella tarda
Parasitic Tilapia guinensis Clinostomum tilapiae, Eye damage, Nigeria Echi et al. (2009)
co-infections C. complanatum and exophthalmia, corneal
Euclinostomum heterostomum. ulceration and
blindness.
Roughening of the
skin by bumps/
yellow grubs
caused by encysting
metacercariae.
Tilapia zilli C. complanatum, C. tilapiae Blindness, myositis and Nigeria Echi et al. (2012)
and Euclinostomum muscle bumps (yellow
hetereostomum grubs)
Nile tilapia Four specimens were infected Infestation of gills, oral Brazil Pinto et al. (2014)
with Centrocestus formosanus cavity and eyes.
and Austrodiplostomum
compactum.
One specimen with
A. compactum and
Drepanocephalus sp..
One specimen with
A. compactum and Ribeiroia
sp.
Nile tilapia G. cichlidarum and C. sclerosus Immunosuppression China Zhi et al. (2018)
characterized by
significant down-
regulated TNF-α,
TGF-β and COX−2
expressions in the
gills.

Note: COX-2: cyclooxygenase-2; TGF-β: transforming growth factor-beta; TNF-α: tumour necrosis factor-alpha
4 | ABDEL-LATIF et al.

TA B L E 2 Potential co-infections with two or multiple different pathogens in tilapia species and their pathogenic effects

Synergistic The co-infecting

co-infections Tilapia species pathogens Pathogenic effects Study area Reference

Parasitic and Nile tilapia G. niloticus and S. iniae Parasitism increased the fish Auburn, USA Xu
bacterial susceptibility and mortality et al. (2007;
co-infections following immersion infection Shoemaker
with S. iniae et al. (2008)
Nile tilapia I. multifiliis and S. iniae The load of I. multifilis and Auburn, USA Xu et al.
trophont size increased (2009)
susceptibility and mortality of
tilapia to S. iniae
Nile tilapia F. columnare and Mass mortalities among Egypt Eissa et al.
Myxobolus tilapiae population. (2010)
Nile tilapia Ectoparasites such Decrease in vaccine performance Auburn, USA Martins et al.
as Trichodina of S. iniae for fish that were (2011)
heterodentata, parasitized with these
G. cichlidarum and ectoparasites.
I. multifilis
Bacteria such as S. iniae
Hybrid tilapia F. columnare after I. multifiliis parasitism of tilapia Auburn, USA Xu et al.
(O. niloticus × O. aureus) parasitism by enhanced F. columnare invasion (2014)
I. multifiliis and resulted in higher mortality.
significantly higher mortality
(60.4%) when exposed
to F. columnare than non-
parasitized fish (29.1%).
The bacterial loads of
F. columnare in fish infected by
I. multifiliis were 13- to 17-fold
higher than those of non-
parasitized fish.
Hybrid tilapia F. columnare and Formalin treatment for Trichodina Auburn, USA Xu et al.
(O. niloticus × O. aureus) Trichodina sp. sp. parasitism reduced bacterial (2015)
infection as suggested by
reduced loads of bacteria in
fish tissues and subsequently
decreased fish mortality
Nile tilapia Bacteria such as Generalized septicaemic signs Egypt Nofal and
V. alginolyticus, with significant mortalities Abdel-Latif
V. harveyii, E. faecalis (2017)
and A. hydrophila
Ectoparasites such as
I. multifiliis, Trichodina
sp. and Gyrodactylus sp.
Nile tilapia A. hydrophila and Heavy mortalities during summer Egypt Abdel-Latif
G. cichlidarum and Khafaga
(2020)
Bacterial Nile tilapia Iridovirus Heavy loss of cultured tilapia Thailand Dong et al.
and viral F. columnare, A. veronii, farms (2015)
co-infections S. agalactiae,
Plesiomonas shigeloides
and V. cholerae.
Nile tilapia Tilapia lake virus (TiLV) Sudden summer high mortalities Egypt Nicholson
and Aeromonads with obvious septicaemic signs et al. (2017)
spp. (A. veronii,
A. ichthiosmia,
A. enteropelogenes and
A. hydrophila)

(Continues)
ABDEL-LATIF et al. | 5

TA B L E 2 (Continued)

Synergistic The co-infecting

co-infections Tilapia species pathogens Pathogenic effects Study area Reference

Red hybrid tilapia TiLV and A. veronii Mass kills with obvious Malaysia Amal et al.
(O. niloticus × O. mossambicus) septicaemic signs. (2018)
Nile tilapia Infectious spleen Outbreaks of massive mortalities Ghana Ramírez et al.
and kidney necrosis (2019)
virus (ISKNV) and
S. agalactiae
Nile tilapia and red hybrid TiLV and A. hydrophila 31% of the naturally examined Thailand Nicholson
tilapia (Oreochromis spp.) fish had TiLV-A. hydrophila et al. (2019)
co-infection.
93% cumulative mortality in
experimental co-infection
compared with 0%, 34% and
6.7% in the control, single
TiLV and single A. hydrophila
infection, respectively.
Serious histopathological findings
were reported in co-infection
compared with single infection.
Fungal and Nile tilapia Pseudomonas Mid-winter mass kills Egypt Eissa et al.
bacterial fluorescence and (2013)
co-infections Candida albicans
Nile tilapia Fusarium oxysporum with Skin and subcutaneous mycoses Spain Cutuli et al.
A. hydrophila with a characteristic granuloma (2015)
formation
Nile tilapia S. iniae and Candida Severe clinical signs, post-mortem Egypt Oda et al.
albicans changes and histopathological (2016)
changes with significant high
mortality rate.
Mixed Nile tilapia and red hybrid Viruses as TiLV. High mortality rates among Thailand Surachetpong
co-infections tilapia Bacteria such as tilapia farms (20%–90%) et al. (2017)
Flavobacterium, especially in fish weighing
Aeromonas and 1–50 g
Streptococcus.
Ectoparasites such
as Gyrodactylus,
Dactylogyrus and
Trichodina sp.

Another case of natural bacterial co-infections was reported in
Nile tilapia where A. jandaei and A. veronii were isolated from Nile
tilapia that had suffered heavy mortalities following transport (Dong
et al., 2017). These authors confirmed the virulence of both aero-
monads through an artificial challenge, whereas the experimental
challenge led to acute mortalities with histopathological findings
characterized by severe congestion and haemorrhages in various or-
gans alongside signs of enteritis (Dong et al., 2017).
Similarly, a case of concurrent infection involving A. hydrophila and
E. tarda was reported from farmed red hybrid tilapia (Lee & Wendy,
2017). The co-infected fish showed loss of pigmentation, exophthal-
mia, corneal opacity and abdominal dropsy with significant mortality.
Both bacteria were found to be resistant to several antibiotics, includ-
ing novobiocin, ampicillin, spiramycin and chloramphenicol. However,
they remained highly sensitive to sulphamethoxazole, flumequine,
oxytetracycline, doxycycline and oxolinic acid (Lee & Wendy, 2017).
In Thailand, a natural case of vertical transmission and co-infec-
tions with Fno and Shewanella putrefaciens was reported for the first
time from red tilapia (Oreochromis spp.) broodstock (Pradeep et al.,
2017). The authors' findings showed that both Fno (6/10) and S. pu-
trefaciens (4/10) were transmitted vertically to the fertilized eggs. In
addition, both bacteria were found at relatively high levels in water
samples from broodstock tanks and larval rearing tanks and both
bacteria could be isolated from tissues and organs of healthy tilapia
broodstock even in the absence of clinical signs demonstrating the
possibility of being carriers to these bacteria.
A recent study on hybrid red tilapia (O. niloticus × O. mossambi-
cus) chronically infected with Fno showed that experimental infec-
tion with S. agalactiae resulted in an outset of mortality that was
more rapid and at a significantly higher rate than the fish without
the secondary infection (Sirimanapong, Thompson, Shinn, Adams, &
Withyachumnarnkul, 2018). The authors showed that infection with
6 |
Fno resulted in acute reduction in the red blood cell (RBC) count
and anaemia, presumably because of damage to the erythropoietic
tissue in the anterior kidney, and theorized that this contributed to
make the fish more sensitive to the secondary infection.
Moreover, a substantial increase in immunological parame-
ters, such as plasma lysozyme and peroxidase activities, was found
with a more pronounced increase in the respiratory burst activity
in the head kidney-derived macrophages in Fno-infected fish that
were experimentally challenged with S. agalactiae than in Fno-
uninfected fish that were experimentally challenged with S. agalac-
tiae (Sirimanapong et al., 2018).
In Brazil, the first case of natural bacterial co-infections in farmed
Nile tilapia has been reported (Delphino, Leal, et al., 2019). These
authors reported on the seasonal dynamics of the bacterial patho-
gens infecting farmed Nile tilapia to identify factors contributing to
the outbreak of the disease in tilapia farms and determine the pos-
sibility of development of potential effective control measures for
improving the fish health. During their follow-up survey, they iden-
tified about 33 cases of Nile tilapia with natural co-infections with
two or three bacterial pathogens such as S. agalactiae, S. iniae, Fno,
A. hydrophila, Pleisiomonas shigelloides and E. tarda. These co-infec-
tions were associated with several mortalities and may be facilitated
by a combination of several risk factors, such as water temperature
and stress caused by high stocking density and frequent handling
(Delphino, Leal, et al., 2019).
2.2 | Parasitic co-infections
Numerous parasites, especially monogenetic and digenetic trema-
todes, and ciliated protozoans have been identified in tilapia. For
example, the monogenetic trematode Cichlidogyrus has been iso-
lated and described from the gills of cichlids (Arthur & Lumanlan-
Mayo, 1997; Paperna, 1996). Other Cichlidogyrus species have been
described from tilapia such as C. sclerosus and C. tilapiae (Le Roux &
Avenant-Oldewage, 2010). In addition, gyrodactylid parasites such
as Gyrodactylus cichlidarum are one of the main monogenean species
infecting juvenile Nile tilapia and could lead to severe mortalities
of intensively farmed fish worldwide (García-Vásquez et al., 2010).
Among the digenetic trematodes that infect tilapia and cause
several disease problems are Clinostomum and Euclinostomum.
Clinostomum tilapiae and C. complanatum have been identified in
the intestine of Nile tilapia and Sarotherodon galilaeus (Ukoli, 1966).
These digenetic metacercariae have been found to be encysted in
tilapia tissues such as the submucosa of the mouth cavity, the gill
chamber, the operculum, the muscles, abdominal cavity, mesentery
and viscera (Chung, Kong, & Moon, 1995). The encysted metacer-
cariae of Euclinostomum heterostomum were also recorded in tilapia
in Egypt (Eissa, Gado, Laila, Zaki, & Noor El-Deen, 2011).
Moreover, ectoparasite infestation with ciliated protozoans, such
as Trichodina sp. and Ichthyophthirius multifiliis, has been investigated
and described in tilapia (Pantoja et al., 2012; Shoemaker, Evans, &
Klesius, 2000).
ABDEL-LATIF et al.
In the Lake Opi, Nigeria, natural cases of parasitic co-infections
involving three clinostomatid parasites have been reported in wild
tilapia, Tilapia guinensis (Echi, Okafor, & Eyo, 2009) and T. zilli (Echi,
Eyo, Okafor, Onyishi, & Ivoke, 2012), and have been linked to serious
disease problems. Similarly, the metacercariae C. tilapiae, C. compla-
natum and E. heterostomum were described together in co-infected
fish and their presence was reported in various tissues and organs of
the affected fish, in particular the buccal cavity, eye, skin and gills.
This was associated with obstruction of the branchial blood circula-
tion followed by asphyxiation and death with marbled gills due to the
presence of yellow grubs. The affected fish exhibited eye damage
due to corneal infection resulting in exophthalmia, corneal opacity
and ulceration with total blindness. Skin lesions were in the form of
roughening of the skin by bumps caused by encysted metacercariae.
Other cases of metacercarial co-infections were reported in
Nile tilapia fingerlings in Brazil, where 16.2% of the parasitized fish
showed metacercarial co-infection (Pinto, Mati, & Melo, 2014). Four
specimens were found infected with both Centrocestus formosanus
and Austrodiplostomum compactum, one specimen with A. compac-
tum and Drepanocephalus sp., and one specimen with A. compactum
and Ribeiroia sp. The presence of metacercariae was demonstrated
in the gills, oral cavity and eyes (Pinto et al., 2014).
Furthermore, Zhi et al. (2018) have evaluated and compared
the effects of single parasitic infection with co-infection between
G. cichlidarum and C. sclerosus and the immune response and the ex-
pression of immune-related genes, such as interleukin-1β (IL-1β), tu-
mour necrosis factor-alpha (TNF-α), transforming growth factor-beta
(TGF-β), heat-shock protein 70 (HSP70) and cyclooxygenase-2 (COX-
2), on the exposed Nile tilapia. These authors demonstrated that the
synergistic interaction between the two monogeneans resulted in
immunosuppression with significant down-regulation of the expres-
sion of TNF-α, TGF-β and COX-2 in the gills at day 2 after G. cichli-
darum infection on the skin.
2.3 | Parasitic and bacterial co-infections
Parasites and bacteria are common inhabitants in the water of fish
farms, and it has been suggested that concurrent infections of ec-
toparasites with some bacterial pathogens resulted in a symbiotic
relationship (Eissa et al., 2010). Similarly, it has been shown that co-
infections with G. niloticus and S. iniae in Nile tilapia resulted in sig-
nificant increase in mortalities (42.2%) compared with fish infected
with either S. iniae or G. niloticus alone (6.7% and 0%), respectively
(Shoemaker, Xu, Klesius, & Evans, 2008; Xu et al., 2007). This showed
that parasitism by G. niloticus increased fish mortality, and it is plau-
sible that G. niloticus could act as a vector for S. iniae. Indeed, the
presence of bacteria on the surface of Gyrodactylus has been dem-
onstrated by scanning electron microscopy (Cusack & Cone, 1985).
Furthermore, the attachment of the parasite is known to result in
damage to the surface of the fish and these sites might constitute
portals of entry for the bacterium (Cone & Odense, 1984; Cusack &
Cone, 1985, 1986; Hoffman, 1985).
ABDEL-LATIF et al.
Similar synergy between bacteria and parasites has been pre-
viously reported in other fish species. Co-infections with G. derja-
vini and F. psychrophilum have been described in rainbow trout (e.g.
Busch, Dalsgaard, & Buchmann, 2003). Moreover, parasitism of
channel catfish fry with Trichodina sp. resulted in increased suscep-
tibility of catfish to S. iniae or S. agalactiae (Evans, Klesius, Pasnik, &
Shoemaker, 2007). In addition, elevation in the severity of disease
signs caused by F. columnare has been reported in fish co-infected
with the crustacean parasite Argulus coregoni (Bandilla, Valtonen,
Suomalainen, Aphalo, & Hakalahti, 2006).
Likewise, the mortality of Nile tilapia fry was considerably en-
hanced following co-infections with I. multifiliis and S. iniae (Xu
et al., 2009). Similarly, an enhanced susceptibility of hybrid tilapia
to F. columnare after parasitism by I. multifiliis has been described
(Xu et al., 2014). This is similar to findings in channel catfish,
where theronts and trophonts from I. multifiliis have been shown
to act as a mechanical vector and contribute to the transmission
of E. ictaluri to exposed fish (Xu, Shoemaker, & Klesius, 2012; Xu,
Shoemaker, Zhang, & Klesius, 2013). It is also likely that the stress
from infection leads to a depression of the fish immune response
and increased susceptibility to infection (Bowers et al., 2000; Tully
& Nolan, 2002).
Indeed, the effects of parasitism on the efficacy of vaccina-
tion of Nile tilapia against S. iniae have been evaluated (Martins,
Shoemaker, Xu, & Klesius, 2011). These authors demonstrated that
the vaccinated Nile tilapia experimentally parasitized with T. het-
erodentata, G. cichlidarum and I. multifiliis showed lower relative
protection survival (RPS) than vaccinated fish without further par-
asitic infection. This finding is similar to what has been reported in
Atlantic salmon, Salmo salar, where sea louse, Caligus rogercresseyi,
may explain the reduced efficacy of vaccines against the bacterial
pathogen, Piscirickettsia salmonis, in salmon sea cages (Figueroa
et al., 2017).
Moreover, ichthyophthirius has been reported to induce a local
immune response with elevated expression of dermal immunity of ti-
lapia. This is consistent with what has been previously demonstrated
in the skin of rainbow trout, Oncorhynchus mykiss (Sigh, Lindenstrom,
& Buchmann, 2004), and common carp, Cyprinus carpio (Gonzalez,
Buchmann, & Nielsen, 2007a, 2007b).
In Egypt, a mass mortality event during the summer season in the
Sharkia Province has been linked to concurrent infection with both
F. columnare and the myxosporean parasite, Myxobolus tilapiae (Eissa
et al., 2010). This synergy could be explained by the ability of the
myxosporean parasite to secrete proteolytic enzymes, which were
able to digest the entire skin including hypodermis and underlying
musculature, leading to the occurrence of “hole-in-the-head"-like le-
sions (Eissa, Abu Mourad, & Borhan, 2006). This extensive damage
to the fish skin may constitute a site of attachment and be further
amplified by F. columnare (Eissa et al., 2010).
Another study demonstrated that the treatment of Trichodina
sp. with formalin solution will help in the reduction in the load of
F. columnare and subsequently improved the survival rate of hybrid
tilapia (Xu et al., 2015).
| 7
Additionally, multiple bacterial and parasitic infections have been
reported to induce concurrent infections in the earthen pond culture
Nile tilapia in Manzala, Egypt, whereas the examined fish have been
shown to be infected with bacterial infections composed of V. algino-
lyticus, V. harveyii, E. faecalis and A. hydrophila, and several ectopar-
asites such as I. multifiliis, Trichodina sp. and Gyrodactylus sp. (Nofal
& Abdel-Latif, 2017). Diseased tilapia exhibited generalized signs
of septicaemia and suffered significant mortalities. In this case, the
interaction between these pathogens was amplified by stress from
the deteriorated water quality parameters such as elevated ammo-
nia, nitrite, hydrogen sulphide and organic matter. In a recent study,
another natural case of co-infections with A. hydrophila and G. cichl-
idarum was reported in pond-reared Nile tilapia in Behera Province,
Egypt, during summer mortalities (Abdel-Latif & Khafaga, 2020).
2.4 | Bacterial and viral co-infections
Several viruses have been isolated and identified in association with
mortality cases of tilapia species (Machimbirike et al., 2019). Tilapia
lake virus (TiLV) is one of the most devastating viral infections nega-
tively affecting tilapia culture worldwide. It has been associated with
mass kills of tilapia species in Israel and Ecuador (Bacharach et al.,
2016; Del-Pozo et al., 2017; Eyngor et al., 2014; Ferguson et al., 2014),
Colombia (Tsofack et al., 2017), Egypt (Fathi et al., 2017; Nicholson
et al., 2017) and Malaysia (Amal et al., 2018). Furthermore, Iridovirus
is another important virus that has been reported to induce heavy
mortalities in Nile and Mozambique (O. mossambicus) tilapias (Ariel
& Owens, 1997; McGrogan, Ostland, Byrne, & Ferguson, 1998). In
addition, infectious spleen and kidney necrosis virus (ISKNV) firstly
reported in Africa has been linked with mass mortalities in farmed
tilapia (Ramírez-Paredes et al., 2019).
Natural concurrent infections between bacterial and viral patho-
gens have been implicated in the occurrence of serious disease
outbreaks in farmed Nile tilapia (Dong et al., 2015). These authors
reported mass kills in cage-cultured Nile tilapia with a co-infec-
tion with Iridovirus, including F. columnare, A. veronii, S. agalactiae,
Plesiomonas shigeloides and Vibrio cholerae.
In Egyptian tilapia farms, the relationship between the occur-
rence of massive summer mortalities in farmed Nile tilapia and the
emergence of TiLV has not yet been determined (Jansen & Mohan,
2017); however, several reports of TiLV isolation from some Egyptian
farms have been documented from Nile tilapia that experienced
summer mortalities (Fathi et al., 2017; Nicholson et al., 2017).
Numerous cases of TiLV with bacterial co-infections were re-
ported in several tilapia species (Amal et al., 2018; Nicholson et al.,
2017, 2019).
High mortalities among the Egyptian tilapia have been reported
in the summer season (Nicholson et al., 2017). The affected fish
exhibited darkened skin, several haemorrhagic patches, detached
scales, fin rot and open wounds with significant mass mortalities,
and laboratory investigation revealed several bacterial pathogens
involved in a concurrent infection with the TiLV. These bacteria are
8 |
aeromonads including A. veronii, A. ichthiosmia, A. enteropelogenes
and A. hydrophila (Nicholson et al., 2017).
In Malaysia, another case of natural co-infection between the
TiLV and A. veronii has been reported, resulting in high mortality in
farmed red hybrid tilapia (O. niloticus × O. mossambicus) (Amal et al.,
2018). The affected fish displayed lethargy, loss of appetite, surface
swimming, skin redness and haemorrhages, especially at the oper-
cula and at the base of fins. Internally, the gall bladder was enlarged,
and severe haemorrhages were visible on the liver, spleen and kid-
ney. Laboratory diagnosis test conducted on a total of 20 diseased
fish showed an infection rate of about 20% and 50% for TiLV and
A. veronii, respectively (Amal et al., 2018).
Recently, a synergistic natural co-infection between TiLV and
A. hydrophila has been reported, which has not only increased the
mortality in Nile tilapia and red hybrid tilapia (Oreochromis spp.)
but also worsened the disease severity (Nicholson et al., 2019).
About 31% of the examined fish were found to be infected with
both TiLV and A. hydrophila. In addition, this case of co-infec-
tion was reproduced under laboratory conditions and resulted in
93% cumulative mortality compared with 0%, 34% and 6.7% in
the control, single TiLV and A. hydrophila infection, respectively.
Additionally, it was reported that the experimental co-infection
revealed more serious histopathological findings than infections
with individual pathogens.
Previously reported cases of natural co-infections between TiLV
and bacterial infections in tilapia suggest that both may act synergis-
tically to induce heavy mortalities of the exposed fish. However, it
should be noted that the relative importance of TiLV and any other
co-infections in terms of severity, mortality and incubation time
has not been determined (Jansen, Dong, & Mohan, 2019). Most re-
ports of co-infections involving TiLV alongside other bacterial and
parasitic co-infectious pathogens were associated with mortality.
However, these reports had not yet determined the respective role
of the co-infecting pathogens in the disease severity, course and
mortality nor elucidated any synergistic effect.
Recently, natural concurrent infection with ISKNV and S. aga-
lactiae was identified in farmed Nile tilapia, whereas fish showed
darkening of skin coloration and erratic swimming with abdominal
dropsy, and experienced massive mortalities in Lake Volta, Ghana
(Ramírez-Paredes et al., 2019).
2.5 | Fungal and bacterial co-infections
In fish, fungal infections are generally believed to be opportunistic,
related to environmental changes that stress the affected fish or
secondary invaders alongside other infectious pathogens (bacteria
or parasites). However, under some circumstances, some fungi can
possibly induce disease and play a primary role (Salter et al., 2012;
Yanong, 2003). In Nile tilapia, various fungal and bacterial concur-
rent infections have been reported (Cutuli et al., 2015; Eissa et al.,
2013; Oda, Tohamy, & Massoud, 2016).
ABDEL-LATIF et al.
In Egypt, mid-winter mass kills affecting Nile tilapia juveniles
at the Mariotteya Stream were characterized by multiple skin ul-
cers and respiratory and osmoregulatory failure, leading to mass
mortalities. The cause of these mortalities was identified as de-
teriorated water quality worsening a concurrent infection caused
by Pseudomonas fluorescens with a secondary invasion by the yeast
Candida albicans (Eissa et al., 2013). This study was a typical exam-
ple of stress-related nature of fish diseases, whereas the polluted
water with a stagnation of the water stream with a substantial in-
crease in ammonia, phenol and polycyclic aromatic hydrocarbons
with low levels of DO was considered as the initial stimuli for dis-
ease (Eissa et al., 2013). Moreover, C. albicans is known to be able to
colonize the epithelial surface of fish and continue to grow result-
ing in deep penetration into the muscles, tissues and organs (Chen
et al., 2013), which could act as a portal of entry for bacteria. On the
other hand, exotoxins of P. fluorescence have a proteolytic poten-
tial (Thune, Stanley, & Cooper, 1993), which facilitates secondary
fungal infection by C. albicans. In addition, fungal infections occur
after fish have lost their protective mucous (Quiniou, Bigler, Clem,
& Bly, 1998).
In a similar fashion, primary infection with S. iniae followed by
secondary opportunistic infection with C. albicans has also been re-
ported from Nile tilapia (Oda et al., 2016). Clinicopathological find-
ings included respiratory distress, exophthalmia, corneal cloudiness
and deep diffuse ulcerations with significant high mortalities.
The presence of subcutaneous granulomas of Nile tilapia fries
after eight weeks of transportation revealed the presence of co-in-
fections with Fusarium oxysporum and A. hydrophila (Cutuli et al.,
2015). In this case, A. hydrophila was identified as the main cause
of systemic infection with several mortalities (Cutuli et al., 2015). A
similar co-infection with A. hydrophila and Fusarium sp. was reported
in ornamental fish, Symphysodon sp. (El-Ghany, El-Khatib, & Salama,
2014). The scenario of pathogenicity due to combined infections
with F. oxysporum and A. hydrophila in the fries of Nile tilapia may be
attributed to the primary invasion of F. oxysporum that help in facil-
itating the invasion of A. hydrophila by tissue damage (Cutuli et al.,
2015).
2.6 | Mixed and multiple co-infections
In Thailand, multiple outbreaks with heavy mortality (20%–90%)
were reported in Nile tilapia and red hybrid tilapia (Oreochromis
sp.), especially in fish weighing 1–50 g (Surachetpong et al., 2017).
Multiple and mixed infections were involved in these mortalities. It
was found that the emerging devastating TiLV was identified and
phylogenetic analysis showed that this virus was similar to TiLV from
Israel. Additionally, several concurrent infections with bacteria, such
as Flavobacterium, Aeromonas and Streptococcus, and various infesta-
tions by external parasites, such as monogenean parasites includ-
ing Gyrodactylus, Dactylogyrus and ciliated protozoan, Trichodina sp.,
were also implicated.
ABDEL-LATIF et al.
3 | M EC H A N I S M S O F S Y N E RG I S TI C
CO - I N FEC TI O N S
An overview of the possible scenarios associated with synergistic
interactions in tilapia is summarized in Figure 1.
One of the most important effects of co-infections is that the
pathogens might reduce the fish's resistance to other diseases (Bandilla
et al., 2006; Busch et al., 2003; Evans et al., 2007). For example, the
infection with ectoparasites may reduce the barrier immunity and act
as a portal of entry for other co-infecting pathogens. This was the case
in tilapia, where Xu et al. (2009) demonstrated that the infestation of
ichthyophthirius caused the destruction of the protective mucous of
fish and increased the susceptibility to S. iniae infection.
The host immune response may also be affected by co-infec-
tants, which may also alter the host's immune response to sub-
sequent infections by other pathogens either by suppressing or
by priming the immune system (Kotob et al., 2017). This can lead
to a subsequent increase in the severity of infection with a higher
mortality rate (Eissa et al., 2013). For example, suppression of the
localized mucous immunity of Nile tilapia after G. cichlidarum infec-
tion may explain an apparent elevation of the fish susceptibility to
C. sclerosus infection (Zhi et al., 2018). Similar findings were reported
in goldfish, Carassius auratus, infected with Dactylogyrus intermedius
that showed down-regulation of TGF-β expression and became more
susceptible to F. columnare (Zhang et al., 2015).
It has been suggested that synergistic interactions between bac-
terial pathogens resulting in mortalities in hybrid red tilapia were
due to the pathogenic action of Fno resulting in anaemic fish due
F I G U R E 1 A schematic diagram showing the possible
consequences and impacts of synergistic co-infections in tilapia
| 9
to the damage that occurred in the erythropoietic tissue of the an-
terior kidney (Sirimanapong et al., 2018). This anaemia and the loss
of the immune cells would make the exposed fish more susceptible
to secondary infection with S. agalactiae (Sirimanapong et al., 2018).
However, only limited studies have investigated the immunosup-
pressive effects of co-infections and further studies are needed for
proper discussion of the relationship between the occurrence of
co-infections and the depression of host immune responses.
Moreover, immunosuppression can cause vaccines to lose their
protectiveness (Figueroa et al., 2017; Martins et al., 2011). For ex-
ample, it has been demonstrated tilapias vaccinated against S. iniae
and parasitized with several ectoparasites such as Trichodina,
Gyrodactylus and I. multifiliis showed lower relative percentage sur-
vival (RPS) in comparison with vaccinated and parasite-free fish
(Martins et al., 2011). Additionally, the treatment of the ciliated pro-
tozoan, Trichodina sp., with formalin solution leads to minimizing the
bacterial load of F. columnare and it subsequently improved the sur-
vivability of hybrid tilapia (Xu et al., 2015). However, more research
is needed for a better understanding of the immune response of tila-
pia during mixed infections as these could have an important impact
on vaccination efficacy (Delphino, Barone, et al., 2019).
Synergistic interactions between TiLV and other bacterial patho-
gens worsen the disease in tilapia and caused increased mortalities.
The accurate pathogenic mechanism of this interaction was not yet
clearly understood until now, but it has been suggested that primary
TiLV infection caused a weakening in the fish immune system, leading
to increased susceptibility to the secondary infection by A. hydrophila
(Nicholson et al., 2019). In such a case, the bacteria cannot be cleared
by the host immunity and this gives it a chance to proliferate rapidly
due to the failure of the antibacterial immune response. Likewise, in
common carp, it was found that the viral infection caused suppres-
sion of the fish mucin production and this makes it more vulnerable
to secondary bacterial infections (Adamek et al., 2017).
On the other hand, numerous antagonistic interactions between
homologous co-infecting pathogens in several fish species have
been reviewed by Kotob et al. (2017). In these interactions, the
first pathogen triggers and modulates the fish's immune response
and hinders the action of the second pathogen. In farmed brown
trout, Salmo trutta, antagonistic interactions have been reported
between two myxozoan parasites, Tetracapsuloides bryosalmonae
and Chloromyxum schurovi (Holzer, Sommerville, & Wootten, 2006;
Peeler, Feist, Longshaw, Thrush, & St-Hilaire, 2008). Similarly, nu-
merous antagonistic interactions between two co-infecting viruses
were reported in rainbow trout, Oncorhynchus mykiss (Alonso, Saint-
Jean, & Pérez-Prieto, 2003; Brudeseth, Castric, & Evensen, 2002);
Japanese flounder, Paralichthys olivaceus (Pakingking Jr et al., 2003,
2004); and Atlantic salmon, Salmo salar (Johansen & Sommer, 2001).
In tilapia, no instances of antagonistic interactions have been re-
ported during co-infections. It is likely that such instances do occur,
for example between TiLV and other viruses, but these have yet to
be identified. Therefore, future plans and perspectives should be di-
rected for the researchers and scientists to explore such interactions
between the co-infecting pathogens.
10 | ABDEL-LATIF et al.
4 | ECO N O M I C I M P O RTA N C E O F
CO - I N FEC TI O N S I N TI L A PI A
The previously reported cases of natural co-infections in tilapia
act synergistically to worsen the health status of infected fish
and accelerate the course of the disease. Most of the cases re-
sulted in heavy mortalities among infected tilapia, leading to
serious economic problems in tilapia aquaculture. However, the
calculated losses (e.g. financial and production losses) were only
rarely addressed in these studies. Scientists described the eco-
nomic losses caused by co-infections in tilapia based on their
impacts on the affected fish and the recorded mortalities. It has
been demonstrated that co-infections with Clinostomum species,
which is considered as the largest metacercariae affecting fish,
induce a reduction in the marketability and palatability of the in-
fected tilapia species with reported zoonotic transmission with
possible occurrence of pharyngitis in Nigerian people (Echi et al.,
2009, 2012). Concerning the bacterial co-infections in tilapia, a
daily mortality has been recorded for a period of 50 days with a
cumulative mortality in cage-reared tilapia that reached 1.48%,
4.8% and 3.24% in three cages of the surveillance study (Assis,
Oliveira, et al., 2017; Assis, Tavares, et al., 2017). Meanwhile, it
was found that the impairment of vaccine efficacy during natu-
ral bacterial co-infections in tilapia could lead to high economic
losses (Delphino, Barone, et al., 2019).
Bacterial and viral co-infections in tilapia have resulted in cu-
mulative mortality that may reach up to 50% per crop in Thailand
(Dong et al., 2015). Furthermore, it was reported that from about
100,000 pond-reared red hybrid tilapia fries, between 300 and
1,800 fries died daily over the course of three successive weeks
(Amal et al., 2018). Finally, high mortality rates reaching 20%–90%
have been reported from farmed tilapia with body weight ranging
from 1 to 50 g and attributed to mixed and multiple co-infections
(Surachetpong et al., 2017). Nevertheless, more detailed research
focusing on the economic appraisal of these co-infections is
needed to better evaluate the economic losses due to co-infec-
tions in tilapia farming.
5 | CO N C LU D I N G R E M A R K S A N D
FU RTH E R PE R S PEC TI V E S
This article focuses mainly on reviewing several reports of naturally
occurring and experimentally induced co-infections in different
species of tilapias worldwide in order to evaluate their interac-
tions, their effect on the severity of infections and the course of
the disease, and scenarios of pathogenesis responsible for dis-
ease signs and the pathological findings. A particularly common
instance of concurrent infections may be attributed to coloniza-
tion by ectoparasites, which act as a portal of entry for the second
co-infecting pathogen. Suppression of the host immune response
resulting in an enhanced effect of the secondary invaders can also
occur, and both co-infecting pathogens act synergistically to induce
disease with greater economic losses of the affected tilapia. Based
on the existing scientific literature, it is clear that co-infections are
common and important in tilapia and that more research efforts
should be devoted to better understand the possible mechanisms
of interactions between concurrent pathogens. Moreover, fish
managers should remain mindful of the possible occurrence of such
co-infections and take these into consideration, especially during
diagnosis and when designing prevention strategies, and planning
for vaccination.
C O N FL I C T O F I N T E R E S T
The authors declare that they do not have any commercial associa-
tions, current and within the past five years, that might pose a poten-
tial, perceived or real conflict of interest.
DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study and not presented
in the figures, tables and appendices are available upon reasonable
request.
ORCID
Hany M. R. Abdel-Latif https://orcid.org/0000-0001-8761-1493
Mahmoud A. O. Dawood https://orcid.org/0000-0002-4887-8838
Simon Menanteau-Ledouble https://orcid.org/0000-0002-3435-9287
Mansour El-Matbouli https://orcid.org/0000-0001-8148-0218
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