DOI: 10.1002/aff2.200
OR I G I N A L A RT I C L E
Saprolegniosis in aquaculture and how to control it?
Petra Camilla Lindholm-Lehto1 Päivi Pylkkö2
1Aquatic Production Systems, Natural
Resources Institute Finland (Luke), Jyväskylä,
Finland
2Research Infrastructure Services for
Cultivated Fish Stocks, Natural Resources
Institute Finland (Luke), Joensuu, Finland
Correspondence
Petra Camilla Lindholm-Lehto, Aquatic
Production Systems, Natural Resources
Institute Finland (Luke), Survontie 9A,
FI-40500 Jyväskylä, Finland.
Email: petra.lindholm-lehto@luke.fi
Funding information
Natural Resources Institute Finland
Abstract
Saprolegniosis, also called water mould, induces a cotton or wool-like white growth
on fish skin. It can kill fish at all stages of life, from eggs to adults. It is caused by
oomycetes from the genus Saprolegnia and causes fish mortality and huge financial
losses to fish farms and hatcheries. Saprolegnia species are endemic and ubiquitous
in all freshwater habitats around the world. The exposing factors for saprolegniosis
are still largely unknown, but stressors such as temperature shocks, poor water qual-
ity, handling and high fish density have been associated with outbreaks. For decades,
malachite green was the most effective treatment against Saprolegnia infection, but it
has been banned due to its carcinogenic and toxic effects. This has forced farmers to
use alternative disinfection methods against Saprolegnia infection, such as hydrogen
peroxide, formalin, Bronopol, NaCl, acetic acid and ozone, although many may have
safety concerns or are impractical to use. This has led to the investigation of plant-
based compounds with antifungal and antibacterial properties against saprolegniosis.
These include extracts of certain herbs, onion, garlic, extracts of the plant Chrysan-
themum, essential oils of Eryngium campestre, Mentha piperita, Cuminum cyminum and
Thymus linearis, which include a variety of phenolic compounds and fatty acids with
antifungal properties. This review combines the current knowledge regarding the pre-
disposing factors to Saprolegnia infections and current methods to prevent and treat
them, including those under further research. Thus far, many compounds have been
tested and studied, but an effective, suitable and safe compound to treat Saprolegnia
infection remains to be found.
KEYWORDS
fish pathogen, formalin, hydrogen peroxide, oomycete, plant-based treatments, Saprolegnia
parasitica
1 INTRODUCTION
Saprolegniosis is a disease which can kill fish in all stages of life, from
eggs to adult fish (Duan et al., 2018; Hirsch et al., 2008; Ruthig, 2009).
The disease is caused by the oomycetes from genus Saprolegnia (Bruno
et al., 2011; Coker, 1923;Duan et al., 2018), although other Saprolegni-
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© 2024 The Author(s). Aquaculture, Fish and Fisheries published by JohnWiley & Sons Ltd.
aceae such as species from genus Achlya can cause identical symptoms
(Chukanhom & Hatai, 2004; Pavić et al., 2022). It is one of the major
obstacles in fish production worldwide. It poses a serious threat to
many species, including rainbow trout, salmon, tilapia and carp, as well
as amphibians and crustaceans (Lone & Manohar, 2018; Peréz et al.,
2003; Shah et al., 2021).
Aqua. Fish & Fisheries. 2024;4:e2200. wileyonlinelibrary.com/journal/aff2 1 of 22
https://doi.org/10.1002/aff2.200
2 of 22 LINDHOLM-LEHTO and PYLKKÖ
Saprolegniosis, also called water mould, induces a cotton or wool-
like white growth on the fish skin and gills (Yanong, 2003). Lesions are
often initially small and focal, but they rapidly enlarge (Zahran & Risha,
2013), causing epidermal damage and cellular necrosis (Noga, 2010).
Saprolegniosis leads to an impaired ability of osmoregulation, loss of
body fluids and finally respiratory failure (vanWest, 2006). The disease
is lethal inmost cases (Fernandez-Beneitez et al., 2008;Magwaza et al.,
2017; vanWest, 2006).
Saprolegnia spp. is ubiquitous in freshwater ecosystems and is the
main genus of water moulds responsible for significant fungal infec-
tions of freshwater fish and eggs (Pelczar et al., 2008). It causes
significant declines in crayfish, fish and amphibian populations (Bruno
et al., 2011; Liu et al., 2015; Pavić et al., 2021; van denBerg et al., 2013)
and has been recognized as a threat to biodiversity (Fisher et al., 2012;
Gozlan et al., 2014). Continuous infections have led to a decline in fish
populations and species diversity (Romansic et al., 2009). Saprolegnio-
sis has been observed in various fish species, amphibians (Blaustein
et al., 1994), crustaceans (Dieguez-Uribeondo et al., 1994) and aquatic
insects (Sarowar et al., 2013). It also threatens somehighly endangered
species (Fernández-Benéitez et al., 2008; Kiesecker et al., 2001).
Saprolegnia spp. is considered responsible for the decline of natural
and culturedpopulationsof salmonids, cyprinids andacipensers (Johari
et al., 2014; van West, 2006), as well as amphibians, crayfish, crus-
taceans (Hirsch et al., 2008; Kiesecker et al., 2010) and other aquatic
species (vandenBerg et al., 2013; vanWest, 2006). In the environment,
saprolegniosis has been observed (Hussein et al., 2001; Qureshi et al.,
2001) not only in brackish (El-Hissy & Khallil, 1989) and freshwater
environments (El-Hissy et al., 2000) but also in lagoons (Ali, 2005; El-
Hissy et al., 2004). It also occurs frequently in fish hatcheries (Shokouh
Saljoghi et al., 2020), on fish farms, andeven inhobby fish tanks, causing
infections (Hussein et al., 2002; Johari et al., 2014; Okumus¸, 2002).
Saprolegnia spp. has been found worldwide: in most European coun-
tries, China, Japan, Southeast Asian countries, India, North and South
America and parts of Australia (Hatai & Hoshai, 1994; Ravindra et al.,
2022; Rowland et al., 2000; Magray et al., 2019). However, there is
more genetic variation among Saprolegnia strains within each country
than between countries (Elameen et al., 2021). According to some esti-
mates, every freshwater fish is exposed to at least oneoomycete during
its lifetime (Neish, 1997), and about 10% of hatched salmon die due to
Saprolegnia parasitica (Adel et al., 2020; Robertson et al., 2009). In aqua-
culture, Saprolegnia infects especially freshwater-cultured salmonids
such as Atlantic salmon Salmo salar and rainbow trout Oncorhynchus
mykiss but also species like eel, perch and catfish (Bruno et al., 2011;
Das et al., 2012). Saprolegniosis causes mortality and presents a great
threat to animal well-being (Magray et al., 2019; Phillips & Subasinghe,
2008).
Fish are one of the most important food sources in many coun-
tries worldwide (Hussain et al., 2011; Rao, 2023; Rubbani et al., 2011).
Globally, fish resources are declining, driven by economic and human
population growth (Limburg et al., 2011). This has led to increased fish
farming,which has become a commercially important industry and sec-
tor in food production worldwide (Shah et al., 2021). Over the years,
production has intensified but has unfortunately led to more disease
outbreaks (El Gamal et al., 2023; Shaheen et al., 2015), which are
problematic for aquaculture and its development (Shah et al., 2021;
Shokouh Saljoghi et al., 2020).
Fish diseases are a major cause of financial losses in aquaculture.
Oomycete (including water mould) infections have the second biggest
impact after bacterial diseases (Johari et al., 2014). Saprolegnia and
Achlya are the two typical species infecting fish and causing sapro-
legniosis (Mastan, 2015). Both cause fish mortality and huge financial
losses to fish farms and hatcheries (Duan et al., 2018; Mostafa et al.,
2020; Songe et al., 2016; Thoen et al., 2011) worldwide (Pavić et al.,
2022). According to some estimates, saprolegniosis causes losses of
billion dollars in Atlantic salmon, rainbow and brown trout and other
species (Bruno et al., 2011; Van West, 2006). For example, in channel
catfish (Ictalurus punctatus), saprolegniosis causes losses of approxi-
mately $40 million in the United States (Bruno et al., 2011; Liu et al.,
2015). In India, disease incidences of S. parasitica have become more
common in thewidely raised striped catfish (Pangasianodon hypophthal-
mus) in recent decades and caused major financial losses on fish farms
and damage in natural ecosystems (Ravindra et al., 2022; van West,
2006).
Thus far, a safe and effective treatment for saprolegniosis has yet
to be established. Previously used and relatively effective treatments
have been banned due to their carcinogenic or toxic properties (Cor-
coran et al., 2010; Mostafa et al., 2020), and it is planned to ban
other treatment chemicals in the future (Bruno et al., 2011). How-
ever, promising results have been received by a selective breeding
programme for Atlantic salmon S. salar (Misk et al., 2022), which indi-
cated lower mortality for Saprolegnia infection in fish from resistant
families.
As early as 2000, Rowland et al. (2000) published an extensive study
of infectious diseases in silver perch (Bidyanus bidyanus), including
saprolegniosis, which contained an extensive section on therapeutic
chemicals. However, this review concentrated on the treatment of
warm water species in Australia. Recently, Barde et al. (2020) have
reviewed saprolegniosis, its taxonomy and life cycle but only briefly
mentioned other treatments besides the banned malachite green.
Buchmann (2022) reviewed methods to control all parasitic diseases
in aquaculture, whereas Tedesco et al. (2022) reviewed natural com-
pounds with therapeutic effects against Saprolegnia spp. Furthermore,
He et al. (2023) extensively reviewed strategies to treat malachite
green residues in the environment. However, a recent and comprehen-
sive study of the known factors affecting saprolegniosis in aquaculture
has been lacking.
The initial cause of saprolegniosis outbreak is still unknown, but
stressors, such as poor water quality, handling and high fish density,
have been associated with disease outbreaks (Whistler, 1997; Zahran
& Risha, 2013). Based on this, this study reviews the currently known
causes and affecting factors of Saprolegnia infections in aquaculture,
focusing on water quality and stressors which may occur in aqua-
culture. Additionally, previously used, current and recently studied
methods have been reviewed for treating saprolegniosis.
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LINDHOLM-LEHTO and PYLKKÖ 3 of 22
2 SAPROLEGNIA SPP
2.1 Classification
Fungal pathogens which infect freshwater fish belong to the
oomycetes class (Daugherty et al., 1998). Oomycetes are taxo-
nomically distributed into three subclasses: Rhipidiomycetidae,
Peronosporomycetidae and Saprolegniomycetidae. Animal pathogenic
oomycetes belong to Saprolegniomycetidae (Jiang et al., 2013; van
West, 2006) which consist of Leptomitales and Saprolegniales (Hart &
Reynolds, 2002; Magray et al., 2019). The Saprolegniales include eight
genera: Saprolegnia, Achlya, Aphanomyces, Calyptratheca, Thraustotheca,
Leptolegnia, Pythiopsis and Leptomitus. The three first are the most
common in causing saprolegniosis in aquaculture (Bly et al., 1994;
Hatai &Hoshiai, 1993; Rao, 2023).
Saprolegniaceae were first introduced by Ledermüller in 1760
(Magray et al., 2019). The classification for the Saprolegnia spp. group
is as follows: kingdom: Chromista (Stramenopiles), phylum: Oomycota,
class: Oomycetes, order: Saprolegniales, family: Saprolegniaceae and
genus: Saprolegnia (Beakes & Ford, 1983;Magray et al., 2019).
Saprolegnia spp. is both saprobic and parasitic, which means that it
obtains nutrition from decaying organic matter and from living hosts
(Seymour, 1970). Previously, oomycetes, fungal-like eukaryotes, were
classified as fungi due to their filamentous growth, because they live
on decayingmatter (Duan et al., 2018). However, they aremore closely
related to algae due to their bi-flagellated zoospores, gametangial cop-
ulation, cellulose cell wall structure and biochemistry (Duan et al.,
2018; Paul & Steciow, 2004). Currently, oomycetes are included in
brown algae and diatoms (Beakes et al., 2012; Derevnina et al., 2016;
Duan et al., 2018).
2.2 Reproduction of S. parasitica
Oomycetes are a widespread group of parasites (Carris et al., 2012;
Rezinciuc et al., 2018). Oomycetes are considered successful because
they can overcome host resistance and even jump to new hosts
(Derevnina et al., 2016). They also have a flexible mating system and
reproduce sexually, asexually, or through interspecific hybridization
(Hardham, 2001). They rely on asexual secondary zoospores (Kim &
Judelson, 2003;Walker& vanWest, 2007)which form cysts and attach
to their hosts prior to the infection (Raftoyannis & Dick, 2006). The
descriptions of developmental stages of oomycetes, including primary
and secondary zoospores, primary and secondary cysts, and germi-
nated cysts, are often shown in a schematic diagram of the oomycetes’
life cycle (e.g., in Mueller, 1994; van West, 2006). Oomycetes can
invade a wide range of hosts, including fungi, algae, plants, inverte-
brates and vertebrates (Robold & Hardham, 2005; Zhang et al., 2013).
They have adaptable mechanisms for host colonization. They con-
tain diverse molecules of translocated host-targeting proteins (Wawra
et al., 2012), the degrading enzymes glycosyl hydrolases and proteases
(Jiang et al., 2013), or adhesive biopolymers (Epstein & Nicholson,
2006). In close proximity to a potential host, oomycetes release effec-
tor proteins and toxins into the host tissues to manipulate their
immune responses (Bly et al., 1992, 1993).
Among the oomycetes, S. parasitica is one of the most harmful fish
pathogens (Magray et al., 2021;Matthewset al., 2021). Thepresenceof
oomycetes in an aquatic environment is one of themost important rea-
sons for saprolegniosis (Bly et al., 1992, 1993). S. parasitica can infect a
wide range of hosts, including important species raised for food (Jaies
et al., 2020;Magray et al., 2021).
Saprolegnia spp. development begins with a slight enlargement of
the terminal portion of a hypha and cytoplasm and nuclei accumulate
in the enlarged tip, called the sporangium, which produces masses of
zoospores (Rao, 2023). Saprolegnia spp. proliferates rapidly at low tem-
peratures and produces zoospores (Matthews, 2019). The tip of the
sporangia breaks down and releases the primary zoospore, which has
two flagella at the anterior end. They move independently for some
time and then encyst. The cyst germinates after a period into hyphae
or bursts to release secondary zoospores, which are reniform with
two flagella laterally placed on the concave side (Rao, 2023). After
swimming for some time, theyencyst and finally germinate intohyphae.
Sexual reproduction in Saprolegnia spp. takes place by the sex organs
developing at tip of the hyphae (Rao, 2023). The female organ oogo-
nium is a globose body, and the male organ antheridium is slender and
sinuous. Sexual reproduction occurs by gametangia contact, in which
the fusion of the haploid oosphere occurs with nuclei, producing a
zygote (Beakes & Gay, 1977). The zygote then transforms into a spo-
rangium, inwhich theprotoplast divides into several zoospores. It takes
nearly 3 months from fertilization to germination into hyphae (Rao,
2023).
Saprolegnia spp. has various components on its cell wall. The major
ones are cellulose, β-(1→ 3)- and β-(1→ 6)-glucans and chitin in small
amounts (Parra-Laca et al., 2015; Rzeszutek et al., 2019). Chitin con-
tributes tomechanical strength to intracellular turgorpressure, playing
an important role inmycelial tip growth (Guerrieroet al., 2010). The cell
wall molecules can evoke immune response in a host (Parra-Laca et al.,
2015). Long zoospores with hook-like end-structures aid its attach-
ment to the host (van West, 2006). In S. parasitica, the zoospores may
be generated repeatedly for up to six generations by a process known
as repeated zoospore emergence (Robertson et al., 2009; van West,
2006).
2.3 Infection
Saprolegnia spp. infects different organisms, including insects, fish,
amphibians and turtles (MacGregor, 1921). The infection can also
be transmitted between species or via contact with infected soil
(Kiesecker et al., 2001). Adhesive compounds allow attachment to the
cell substratum and prevent the removal of pathogen (Bechinger et al.,
1999; Rezinciuc et al., 2018). Biological attachment is based on adhe-
sive polymers which vary in structure and capabilities. S. parasitica
contains hooked hairs or spines on the secondary cysts to attach to fish
(Rezinciuc et al., 2018; Wood et al., 1988). The hooked hairs are more
than 2 μm long, organized in bundles and are rapidly formed during
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4 of 22 LINDHOLM-LEHTO and PYLKKÖ
F IGURE 1 Figures of arctic char (Salvelinus alpinus) infected by saprolegniosis.White lesions occur around the fins and head. Source: Photos by
Juha-Pekka Turkka, Natural Resources Institute Finland.
secondary cyst formation (Beakes, 1983; Beakes et al., 1994). The bun-
dles of hooked hairs are involved in pathogen attachment, and the
strengthof cyst attachmentof Saprolegnia spp. appears tobe correlated
with the lengthof bundles (Pickeringet al., 1979;Rezinciuc et al., 2018).
Additionally, themore efficient attachment of S. parasitica cystsmay be
due to the different stickiness properties and composition of the cyst
extracellular matrix compared to other Saprolegnia species (Rezinciuc
et al., 2018).
Once Saprolegnia spp. has infected its host, it transfers effector pro-
teins into the tissues of the host andmanipulates its immune responses
(Wawra et al., 2012) and can induce perceptible changes in the gills and
kidney (Belmonte et al., 2014), taking the form of profusely branched,
non-septate mycelia. Infected organisms become covered with white
hyphal filaments (Blaustein et al., 1994), which can spread via con-
tact with growing hyphae or through colonization by free-swimming
zoospores (Wood & Willoughby, 1986). The early legions are grey or
white and often appear as circular colonies. They form white cotton-
wool-like tufts or fungalmats in deep skin lesionson fish,whichbecome
grey as cysts are produced (Eissa et al., 2013; Mahfouz et al., 2019).
White or grey mycelium patches on the skin may also penetrate the
muscles (Mahfouz et al., 2019). Mycelia can colonize eggs and lead to
their suffocation and death (Cao et al., 2012; Mousavi et al., 2009). In
severe cases, the lesions can cover 80% of the body. Saprolegnia spp.
typically penetrates the superficial musculature, but in some cases, it
can be even deeper. More rarely, the Saprolegnia spp. can be located
on the oesophageal or gill region of fish. Furthermore, epithelial dam-
age on skin, gills and gut, or other pathogens can offer a route of entry
(Roberts, 2001).
Saprolegnia infection can occur in almost any part of the fish’ body,
but someareas aremore easily infected (Pickering&Willoughby, 1982;
Richards & Pickering, 1978). The pathogen primarily affects epidermal
tissues, fins or head and eventually spreads over the entire surface of
the fish’s body (Figure 1). It may also spread to internal organs liver,
kidney and alimentary canal (vanWest, 2006). Male fish are more vul-
nerable along the dorsal surface, females on the caudal and ventral fins.
There are usually only weak inflammatory responses in the tissues of
the fish. The site of infection and the patterns may vary between farm-
raised and wild fish (Beakes, 1983; Pickering &Willoughby, 1982), and
fish reared in a hatchery are typically infected around the fins. Saproleg-
nia infections are often restricted to the epidermis, dermis and, in some
cases, the superficial musculature (Pickering & Richards, 1980).
The degenerative changes in tissues may represent damage caused
by proteolytic enzymes in the fungal hyphae (Figure 2, Pickering &
Willoughby, 1982; Roberge et al., 2007). Themost harmful effect of the
infection is related to the osmoregulatory system of the fish. Teleost
fish are constantly subject to an osmotic flux of water and loss of ions
across the gills. These are normally balanced by the uptake of salts
and production of urine but require the skin to form an impermeable
layer (Evans, 2008; Pickering & Willoughby, 1982). After a Saproleg-
nia infection, the osmotic pressure and salt content of the blood are
inversely related to the severity of the infection (Richards & Pickering,
1979). The Saprolegnia spp. seems to destroy the essential waterproof-
ing properties, resulting in a lethal dilution of body fluids (Pickering &
Willoughby, 1988).
The changes beneath the skin surface include dermal necrosis
and oedema and in later stages, extensive haemorrhage and deeper
myofibrillar necrosis (Hatai & Hoshai, 1994). The tissue damage is
probably caused by a proteolytic chymotrypsin-like enzyme in the
Saprolegnia spp. (Mueller, 1994). The ultimate cause of death is the
severe hemodilution caused by haemorrhage and the destruction of
the water-proofing properties of the fish’s integument (Pickering &
Willoughby, 1988).
Das et al. (2012) studied the pathogen causing mortality in Indian
major carp (Catla catla) fingerlings. They observed that from the onset
of infection, fish diedwithin 12–15days. The first signswere visible red
or grey patches of filamentous mycelium. The development of patches
was probably due to the rubbing of the body against a hard surface
due to the attachment of filamentous mycelium, which causes itching.
During an acute infection, which took 7–8 days from the beginning of
infection, a cotton-like structure appeared that radiated out in circu-
lar, crescent-shaped, orwhorled pattern (Das et al., 2012). The fish died
within 3–4 days.
Saprolegnia spp. invades epidermal tissues, generally beginning on
the head or fins, and spreads over the entire surface of the body (Neish,
1997;Willoughby & Roberts, 1992; Zaki et al., 2008). Das et al. (2012)
observed that the red patches first appeared in the middle part of the
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LINDHOLM-LEHTO and PYLKKÖ 5 of 22
F IGURE 2 Scanning electronmicrogram (SEM) figures of fish skin infected by saprolegniosis: mycelium-infected epidermis (top), empty
zoosporangium and hypha (bottom left) and a cyst (bottom right) of Saprolegnia parasitica (Roberge et al., 2007).
surface of the body and then gradually spread to other parts. Infec-
tions on fish often occur in the epidermis and dermis but sometimes
in the superficial musculature. Fungal infection eventually destroys
the osmoregulatory system and causes a lethal dilution of body fluids
(Pickering&Willoughby, 1988). Saprolegniosis also causes skin lesions,
erratic swimming behaviour and sunken eyes (Majhi et al., 2005). As a
fungal infection can be seen by the naked eye, a fungal reproductive
process has been initiated, and natural recovery is highly unlikely (Das
et al., 2012).
3 PREDISPOSING FACTORS TO
SAPROLEGNIOSIS
3.1 Stressful conditions
Thus far, the initial cause of saprolegniosis outbreak is unknown.Many
stressors, such as an unsuitable water temperature, poor water qual-
ity, handling and high fish density, have been associatedwith outbreaks
(Whistler, 1997; Zahran & Risha, 2013). However, longitudinal studies
of abiotic and biotic factors remain rare (Duan et al., 2018). Numer-
ous studies have been conducted, but the prevalence of S. parasitica in
the environment or ecological parameters influencing its occurrence
remain very limited (Elameen et al., 2021; Masigol et al., 2020). It
is unclear why some farms have frequent outbreaks, whereas others
remain disease-free.
In aquaculture, numerous factors are involved in the formation
of saprolegniosis, but Saprolegnia-associated mortality appears to
increase in the presence of abiotic stressors (Kiesecker et al., 2001).
For example, overcrowding, an insufficient water flow rate, low oxy-
gen content, poor water quality, injuries from handling, malnutrition,
crowding, stress, temperature shocks, spawning, external parasitism,
or infrequent removal of dead fish or eggs can lead to disease occur-
rences (Pavić et al., 2021; Piper et al., 1982; Bruno et al., 2011; Tedesco
et al., 2022). High stocking densities and injuries formed in inten-
sive breeding techniques have increased the occurrence of mycotic
diseases, including saprolegniosis (Olah & Farkas, 1978).
Stressful rearing conditions (temperature shocks, infections by bac-
teria and fungi, pollutants, overcrowding, injuries from biting and due
to rough handling and transportation, low levels of dissolved oxygen,
temperature fluctuations, osmotic shocks and poor water quality) can
weaken the immune system of the reared species and increase suscep-
tibility to S. parasitica (Bly et al., 1993; Hatai & Hoshiai, 1994; Howe
& Stehly, 1998; Pavić et al., 2021; Roberge et al., 2007). Insufficient
removal of dead fish and eggs can result in a higher spore load and act
as a predisposing factor for saprolegniosis (Bruno et al., 2011; Tedesco
et al., 2022).
Saprolegniosis is a commonproblem for salmonand trouthatcheries
and is often associated with broodstock, fertilized ova and parr (Hatai
& Hoshiai, 1993), especially when wild or broodstock fish are held
and handled for the taking of eggs or milt (Howe & Stehly, 1998).
Hatchery managers often need to treat fish regularly with an antimi-
crobial or anti-oomycete chemical during stressful periods to prevent
saprolegniosis.
Stress related to increased water temperatures can increase
susceptibility to saprolegniosis (Casas-Mulet et al., 2021;
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6 of 22 LINDHOLM-LEHTO and PYLKKÖ
Stewart et al., 2018) but also transformation to different life stages
(Pickering, 1994). Pickering (1993) concluded that stress stimulates
the hypothalamic-pituitary-interrenal axis of salmonids and leads
to increased cortisol levels. It is an immunosuppressant and prob-
ably causes the suppression of the defence system, increasing the
stress-induced likelihood of saprolegniosis (Pickering, 1994).
Incorrect handling procedures can lead to damage to the fish skin
and increased stress, which are both associated with a higher suscep-
tibility to saprolegniosis (Beckmann et al., 2020; Bruno et al., 2011).
Pavić et al. (2022) observed and reported how the health status of the
fish significantly influenced S. parasitica on the skin of injured rainbow
O.mykiss and brown trout Salmo trutta, which had significantly higher S.
parasitica loads than the apparently healthy fish.
Both abiotic and biotic stressors may act synergistically with
pathogens to increase the adverse effects on hosts (Romansic et al.,
2006). If both pathogens and stressors are present, the effects on hosts
may be more aggravated than when either is present alone (Khan,
1990). Saprolegniosis can also be a secondary to viral or bacterial infec-
tion (O’Brien, 1974), or fish can be impacted by several pathogens
(Daszak et al., 2003), and the effects are influenced as co-factors
(Christin et al., 2003; Kiesecker, 2002). Additionally, an inadequate
diet and nutritional deficiencies also play a role. An insufficient sup-
ply of ascorbic acid is especially important for collagen production and
for sufficient mucus production and tissue regeneration (Ashley et al.,
1975; Pavić et al., 2022).
The quality and quantity of mucus in various parts of the fish’s body
may play a role in saprolegniosis (Noga, 1993). Mucus concentration
tends to be lower on the fins than on the remaining sites on the fish’s
body, allowing faster zoospore attachment to the fins than the rest of
body (Durborow et al., 2003; Richards & Pickering, 1978).
The control of saprolegniosis depends on good husbandry practices
in hatcheries and on fish farms. It includes the prevention of pathogens,
the maintenance of good water quality, a decrease of environmental
stressors, adequate nutrition (Meyer, 1991; Tedesco et al., 2022) and
proper handling (Ali et al., 2019; Rao, 2023). The defence systems of
fish include enforcement of their immune system andmucus formation
on skin, which play a role in the prevention of saprolegniosis (Quiniou
et al., 1998;Mueller, 1994).
3.2 Water quality
According to the current understanding, water quality influences out-
breaks of saprolegniosis. Previous studies have shown that varying pH,
O2 and total ammonium nitrogen have no direct effect on the devel-
opment of saprolegniosis (Bly et al., 1993), but environmental factors
such as water temperature, salinity and microorganisms seem to be
connected with outbreaks (Mifsud & Rowland, 2008). Saprolegnia spp.
strains grow well at wide temperatures and pH ranges (5–40◦C, pH
2–11, Olah & Farkas, 1978). However, zoospore production decreases
when the water temperature increases above 20◦C, and their germi-
nation is inhibited in acidic (pH < 4) conditions (Dieguez-Uribeondo,
1995; Kitancharoen et al., 1996; Pavić et al., 2021). Additionally, pH
can affect zoospore growth: abundant hyphae at low pH and spherical
schizons at neutral pH (Kocan, 2013;Mahboub & Shaheen, 2021).
High organic load and nitrogen compounds have been connected
with Saprolegnia spp. infections (Pavić et al., 2022). Even sublethal
concentrations of ammonia and nitrites can increase the susceptibil-
ity of trout to saprolegniosis (Carballo & Munoz, 1991). Romansic
et al. (2006) reported that the effects of nitrate and Saprolegnia spp.
were synergistic, not additive. They stated that nitrate might decrease
zoospore production or kill zoospores, inducing physiological response
mechanisms in the host which might lead to resistance to Saprolegnia
spp.
Saprolegniosis rarely occurs in seawater because Saprolegnia spp.
cannot survive in themarine environment at a salinity above 1.75% (as
NaCl, Mueller, 1994). As early as 1979, Taylor and Bailey (1979) sug-
gested that seawater was an effective substitute for malachite green
in preventing saprolegniosis. Salt (NaCl) is a safe and inexpensive par-
asiticide and osmoregulatory aid (Mifsud & Rowland, 2008). However,
its controlling effect varieswith fish species, salt concentration and the
strain of oomycetes (Chukanhom & Hatai, 2004; Mifsud & Rowland,
2008). For example, the survival of silver perch treated with 2–3 g L−1
was 100%, but for untreated fish, only 66.7% (Mifsud & Rowland,
2008).
A high organic load can be associated with Saprolegnia infections
(Pavić et al., 2022). Organic compounds often include humic sub-
stances (HSs) in natural waterbodies, especially in theNordic countries
(Thorsen, 1999). HSs are complex organic molecules that consti-
tute the main part (50%–80%) of dissolved natural organic material
in freshwater ecosystems (Meinelt et al., 2007; Wetzel, 2001). For
example, concentrations of dissolved organic carbon range from 1 to
100 mg L−1 HS in oligotrophic ecosystems (Steinberg, 2003; Wetzel,
2001). Aquatic HS consist of water-soluble substanceswith carboxylic,
phenolic, quinoid and aliphatic groups, and cations of certain ele-
ments (e.g., Na, K, Mg, Ca, Fe, Al and Cu). HSs are large and complex
organicmolecules, but no specific structural formulas canbe given. Sta-
tistical parameters can be defined based on their molecular weight,
aromaticity and elemental analysis.
HS may act as a natural biocide or herbicide (Karasyova et al.,
2007; Prokhotskaya & Steinberg, 2007). Even antibiotic properties
of humic and fulvic acids have been reported (Gryndler et al., 2005).
The effects of HS on living organisms have been reviewed by Stein-
berg et al. (2006), but not the effects of HS on fungi or S. parasitica.
Meinelt et al. (2007) tested the effects of HS (20 HS and natural
organic matter, NOM) on S. parasitica in vitro. The HSs were collected
and isolated from real aquatic environments in central and northern
Europe and were characterized by high-performance size-exclusion
chromatography. The results of Meinelt et al. (2007) showed that HS
might enhance and reduce the vegetative growth of the water mould
S. parasitica. This is based on NOMs rich in carbohydrates and amino
acids which support fungal growth, whereas humic material with high
aromaticity and high C:H and C:CH2 ratios inhibits the growth of
water mould. Later, Pavić et al. (2022) showed that HSs and other
dissolved organic matter could inhibit mycelial growth (Meinelt et al.,
2007).
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LINDHOLM-LEHTO and PYLKKÖ 7 of 22
There are differences between hosts in their susceptibility to Sapro-
legnia infection (Kiesicker&Blaustein, 1995, 1997). For example,water
temperature, pH, pollutants and exposure to UV radiation can alter
susceptibility to saprolegniosis (Lefcort et al., 1997). For example, El
Gamal et al. (2023) focused on investigating outbreaks on fish farms
rearing tilapia (apart from salmonids, the focus of most studies) that
received untreated water with different contamination loads and its
relationship with saprolegniosis outbreaks. Their paper was the first
to study the link between saprolegniosis and improper water quality
sources used on tilapia farms.
Water parameters such as electrical conductivity (EC), cations Ca2+
and Na+, and anions SO4
2− and Cl− are considered highly relevant for
explaining the S. parasitica load in water (Pavić et al., 2022). NO3− and
F− remained barely below the level of significance,whereasCOD, TOC,
K+, TP, NH4
+, pH and Mg2+ had a smaller influence on the S. parasitica
load (Pavić et al., 2022).
Fluoride (F−) has shown a negative correlation with S. parasitica in
water (Pavić et al., 2022), suggesting an inhibitory effect of fluoride on
S. parasitica. In the environment, excessive fluoride concentrations are
known to affect microbial communities by inducing negative effects on
microbial physiology (Marquis et al., 2003;Mendes et al., 2014). To our
knowledge, no studies have been conducted so far on the toxicity of
fluoride to oomycetes.
The strongest positive correlation with S. parasitica was found with
EC and Ca2+. Pavić et al. (2022) concluded that calcium ions could
positively influence the developmental stages and infection process
of oomycetes (Burr & Beakes, 1994; Rezinciuc et al., 2018). Ca2+ ions
regulate adhesion, encystment and germination processes (Pavić et al.,
2022; Rezinciuc et al., 2018). Additionally, Pavić et al. (2022) showed
thatCa2+ concentrations above average (globalmedian4mgL−1,Wey-
henmeyer et al., 2019) in surface waters favoured the growth of S.
parasitica.
Furthermore, EC, describing the total ion content (mainly Na+, Cl−
and Ca2+), has been found to be positively correlated with the S. para-
sitica load (Pavić et al., 2022). In natural freshwater ecosystems, sodium
and chloride concentrations vary from country to country. In high con-
centrations (above1000mgL−1), sodiumchloride is used as a non-toxic
method to control Saprolegnia sp. Sodium chloride can reduce the for-
mation, release and proliferation of sporangia and the growth of the
pathogen (Ali, 2005; Pavić et al., 2022).
Freshwater aquaculture facilities are often connected with
rivers/streams, suggesting the potential transfer of Saprolegnia
pathogens from fish farms to downstream freshwater environments or
fromwater bodies to farms (El Gamal et al., 2023). The escaping fish or
water drainage from or to fish farms can therefore result in pathogen
transfer with the natural environment.
3.3 Temperature
Temperature as an abiotic stressor in fish is frequently cited as a crit-
ical contributing factor to Saprolegnia infection (Bly & Clem, 1991; Bly
et al., 1992). Saprolegniosis outbreaks often occur when temperatures
are near the physiological low end of a particular fish species. Cul-
tured fish often suffer from saprolegniosis during the winter months
when the temperature falls below 10◦C (Naskar et al., 2005). This
may be due to decreased immunity becausemany oomycetes aremore
active in the coolermonths of the year (Rao, 2023). Different species of
Saprolegnia have different optimal growth temperatures, but increased
concentrations are often found at low temperatures. However, other
studies suggest that specific water temperature was not correlated
with saprolegniosis occurrences but with the change in temperature
(Korkea-aho, Wiklund, et al., 2022; Korkea-aho, Viljamaa-Dirks, et al.,
2022). The change in temperature may lead to stress reactions and
immunosuppression in fish andmore likely lead to saprolegniosis.
Saprolegniosis occursmore frequently inwinter (34%) than in spring
(17%) (Mahboub& Shaheen, 2021). Saprolegnia spp. strains grow faster
at low temperatures and germinate at 5◦C in the early spring. Previous
studies have reported seasonal variation of prevalence of Saprolegnia
spp.: 47% in December and only 9% in August (Das et al., 2012; Mah-
boub & Shaheen, 2021) and for tilapia 88.8%, 93.3%, 88.8% and 84.4%
in December, January, February and March (Abd El-Rahman et al.,
2012). For example, the zoospore levels of Saprolegnia spp. were more
than 5 spores mL−1 in the winter and below 1 spore mL−1 during the
summermonths (Bly et al., 1993).
Saprolegnia spp. has a wide temperature tolerance range, from 3 to
33◦C (Aly & El-Ashram, 2000; Willoughby & Roberts, 1992). Low tem-
peratures in the early spring and late fall can cause saprolegniosis,
therefore referred to as ‘winter kill’ (Bly et al., 1993). Bly et al. (1992)
were the first to report this in channel catfish, I. punctatus. They found
that the syndrome was linked to cold fronts when the water temper-
ature dropped (5–9◦C in 12 h and from 20 to 10◦C in 24 h, Bly et al.,
1992, 1993). A rapid decrease and low water temperature has also
been linked to high levels of zoospores of S. parasitica (Bly et al., 1992;
Zahran & Risha, 2013). The mycelial growth rate of S. parasitica was
highest between 15 and 25◦C and zoospore viability at around 10◦C
(Matthews, 2019).
For example, a sudden decrease in water temperature (from 20 to
<8◦C), coupledwith an increase inwater pH (>9), has caused saproleg-
niosis occurrences in cultured fish (Das et al., 2012). Bruno et al. (2011)
reported that sudden changes in temperature could make fish vulner-
able to saprolegniosis due to the increased physiological stress. Indian
major carp species grew better at temperatures from 26 to 33◦C (Das
et al., 2004), and their feeding, swimming, oxygen consumption and
thermal regulation rates were significantly influenced at low temper-
atures (Das et al., 2012). However, the stress of high temperature and
poor oxygen levels may also induce saprolegniosis (Rao, 2023; Roth,
1972).
Bly et al. (1993) also reported that a rapid drop in temperature led
to immunosuppression in catfish, and the presence of fungal zoospores
led to fungal infections. Similarly, Ravindra et al. (2022) stated that dis-
ease incidences were often associated with stressful conditions such
as a low water temperature, or when the host was immunocompro-
mised (Duan et al., 2018; Van den Berg et al., 2013). The combination
of a rapid drop in temperature and its duration led to a saprolegniosis
outbreak (Bly et al., 1993; Zahran & Risha, 2013).
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8 of 22 LINDHOLM-LEHTO and PYLKKÖ
F IGURE 3 Oxalate and chloride salts of malachite green.
4 TREATMENTS
4.1 Malachite green
Malachite green is a diamino derivative of rosaniline dye (Culp &
Beland, 1996). Malachite green has fungicidal properties, which has
led to its use in controlling Saprolegnia infections in freshwater systems
(Culp & Beland, 1996; Hughes, 1994; Stueland et al., 2005). It was long
considered themost effective treatment (Srivastava et al., 2004).Mala-
chite green was originally used in the dye industry in dying silk, wool,
jute and leather (Merck, 1989), but it has also been used as a medical
disinfectant and anthelmintic (Nelson, 1974). It also serves as an addi-
tive in the paper industry, a pigment in ceramics, and has even been
used as a food colouring agent in milk products in India (Khanna et al.,
1973).
Malachite green has been referred to as basic green 4 based on
its colour index, acryl brilliant green, aniline green, Aizen malachite
green, astramalachite green, Benzal green, China green, benzaldehyde
green, diamond green P extra, solid green 0, light green N and fast
green (Culp & Beland, 1996). The CAS name and number for malachite
green oxalate is N-[4-[[4-(dimethylamino)-phenyl]phenylmethylene]-
2,5-cyclohexadien-1-ylidenel-N-methylmethanaminium oxalate 2437-
29-8 (CI 42000).
In ambient conditions, malachite green is a green crystalline powder
and occurs as chloride and oxalate salts (Figure 3), as a neutral car-
bonol form, or in the reduced leuco form (Culp & Beland, 1996). It is
soluble in water (66.67 g L−1) as chloride salt (Reynolds, 1982), but it
decomposes in air due to oxidation to a diarylketone (Bradley, 1958).
In a neutral aqueous solution, malachite green occurs as dye salt and a
lipophilic carbinol base (Alderman, 1985). The carbinol base is colour-
less and almost insoluble in water (500 μg L−1). In acidic conditions,
malachite green salt occurs as completely ionized (at pH 4), whereas,
in basic conditions (pH 10.1), malachite green exists as the carbinol.
In aquaculture, it was used as zinc-free oxalate, whereas a double salt
with zinc chloride was used as a dye (Culp & Beland, 1996).
Malachite green was first used in aquaculture in 1936 (Foster &
Woodbury, 1936) to control fungi. It has been used routinely since the
1930s due to its efficiency against fungal infections (Schnick, 1988).
Among more than 180 tested antifungal compounds, malachite green
was themost efficient with low toxicity towards fish (Meyer & Schnick,
1989). Besides the prevention of oomycete fungi, malachite green can
control Proliferative kidney disease in rainbow trout (Culp & Beland,
1996).
Malachite green was banned in edible fish in the United States,
Europe (Legislative Decree no. 119/92, Forneris et al., 2003), and
worldwide in 2002 due to its carcinogenic and toxic effects and terato-
genic and mutagenic properties (Duan et al., 2018; Kumar et al., 2020;
Shah et al., 2021; Stueland et al., 2005). This has forced farmers to
use alternative disinfection methods against saprolegniosis (Sandoval-
Sierra et al., 2014). Currently, no sufficiently effective treatment has
been found, which has for its part led to the spread of saprolegnio-
sis (Kumar et al., 2020) and struggle for many fish farmers (Derevnina
et al., 2016). Although malachite green has been banned, and its risks
are known, it is still used as an anti-oomycete chemical in some coun-
tries (Kalatehjari et al., 2015; Sattari & Roustayi, 1999). For example,
it can still be used for ornamental fish (He et al., 2023). To overcome
problems related to Saprolegnia spp., an effective antimicrobial agent
is desperately required which is inoffensive to fish and safe for human
health and the environment (Madhuri et al., 2012).
Malachite green was first detected in fish by Poe and Wilson
(1983). In fish, malachite green is absorbed through the gills and skin,
transformed to the leuco form and stored in the lipid tissue (Culp &
Beland, 1996). Carbinol forms of malachite green are more lipophilic
than its cations. Leucomalachite green is oxidized to malachite green
when frozen. Intact malachite green is excreted quite rapidly, but
leucomalachite green has a half-life of about 40 days.
Exposure to malachite green causes reproductive abnormalities in
rabbits and fish (Meyer & Jorgenson, 1983) and enhances the forma-
tion of hepatic tumours in rats (Fernandes et al., 1991), possibly due to
its structural similarity with other carcinogenic triphenylmethane dyes
(Littlefield et al., 1985). In addition to its carcinogenic and teratogenic
properties, malachite green is capable of intercalating and binding of
DNA (Corcoran et al., 2010; Rosenkranz & Carr, 1971).
4.2 Other chemical treatments
Treatment of watermould infection is very difficult, and legal drugs are
limited (Zahran & Risha, 2013). The currently most applied chemicals
against Saprolegnia spp. are formaldehyde, peracetic acid and hydrogen
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LINDHOLM-LEHTO and PYLKKÖ 9 of 22
TABLE 1 Examples of chemicals and their combinations studied or used as treatment for saprolegniosis, concentrations (mg L−1), effects and
references.
Treatment Concentration Effect in fish/eggs/in vitro Reference
Bronopol (2-bromo-2-nitro-
1,3-propanediol)
10–50mg L−1 MIC
100–250mg L−1 MLC
Growth of Saprolegnia parasitica in
vitro
Stueland et al. (2005)
Bronopol (2-bromo-2-nitro-
1,3-propanediol)
100mg L−1 60min
200mg L−1 60min
Hyphal growth of S. parasitica:
colony radius 0–38.5mm
Colony radius 0mm
Oono andHatai (2007)
Chloramine T (C)+ formalin
(F)
8mg L−1 (C)+ 123mg L−1 (F) Spot disease (Ichthyophthiriasis)
decreased 63% in salmonids
Rintamäki-Kinnunen et al. (2005)
Copper nanoparticles 10mg L−1 Relative S. parasitica colony size
60% of control
Kalatehrjari et al. (2015)
Copper sulphate 20–40mg L−1 45.8%–50.5% survival of sunshine
bass larvae
Straus et al. (2016)
Formaldehyde
Formalin (37% formaldehyde)
1–2mL L−1
0, 50, 100, 150mg L−1
58.6% survival of eggs
67%(0), 35%(50), 29% (100),
40%(150) mortality of rainbow
trout
Forneris et al. (2003) and Gieseker
et al. (2006)
Formaldehyde 40–80mg L−1 76%–97% reduced infection on
rainbow trout
Jaafar et al. (2013)
Hydrogen peroxide 15–30mg L−1 44%–85% reduced infection on
rainbow trout
Jaafar et al. (2013)
Hydrogen peroxide 560mg L−1 for 30min 56% rainbow trout parasite-free Rach et al. (2000)
Malachite greena 10mg L−1 Lowest spore count in vitro Caruana et al. (2012)
NaCl 4 g L−1 for 2min, 3×weekly 50% fishmortality Das et al. (2012)
NaCl+KMnO4 4 g L−1 NaCl for 2min+ 5mg L−1
KMnO4 for 10min
8% fishmortality Das et al. (2012)
NaCl+ ascorbic acid 0.17MNaCl+ 5.68mM
ascorbic acid
Reduced protease activity,
inhibited sporangial formation
Ali (2005)
Ozone 0.01–0.2mg L−1 d−1 42.6%–49.1% survival of eggs Forneris et al. (2003)
Peracetic acid 0.1–0.3mg L−1 42%–94% on rainbow trout Jaafar et al. (2013)
Silver zeolite 600mg L−1, 0.06% 100% inhibition in vitro Johari et al. (2014)
Sodium percarbonate 40–120mg L−1 42%–84% reduced infection on
rainbow trout
Jaafar et al. (2013)
Abbreviations:MIC, minimum inhibitory concentration;MLC, minimum lethal concentration against strains of S. parasitica.
aBannedworldwide in 2002 (vanWest, 2006).
peroxide (Adel et al., 2020). Only a few aquatic anti-oomycete agents
are available, and other options besides malachite green have unfor-
tunately been less effective against Saprolegnia spp. (Table 1). Multiple
chemicals have been tested to control saprolegniosis and other par-
asites, as recently reviewed by Buchmann (2022), but their harmful
effects on farming personnel or the environment often prevent their
wider use (Kumar et al., 2020). Many attempts have been made to
prevent saprolegniosis outbreaks by curative and prophylactic anti-
oomycete chemicals (Hussein et al., 2002). Although many compounds
have been tested and studied, a very suitable and safe compound to
treat saprolegniosis remains to be found (Kumar et al., 2020).
Formalin, an aqueous solution of 37% formaldehyde, is commonly
used (Abd El-Gawad et al., 2015) and fairly effective in treating sapro-
legniosis (Table 1, Das et al., 2012; Mitchell & Collins, 1997). Formalin
is currently registered as a disinfectant and/or parasiticide for use in
aquaculture, depending on country (Leal et al., 2018). Formalin can be
administered by adding formalin directly to fish tank water, including
RAS farms (Noga, 2012), usually at concentrations ranging from 20 to
50mg L−1 (Buchmann, 2022).
Formalin is widely used but is not effective enough to control Sapro-
legnia infections in fish, fish eggs (Bruno et al., 2011; Okumus¸, 2002)
and larvae (Gieseker et al., 2006). In some circumstances, formalin has
been found to be very effective against Saprolegnia infections (Rach
et al., 2005; Schreier et al., 1996). However, there are concerns about
its effects on the environment and the handling personnel (Fitzpatrick
et al., 1995). It currently has a classification as a 1B carcinogen by the
European Commission (EC, 2014), indicating that it may be banned as
a treatment option (Abd El-Gawad et al., 2015; Bruno et al., 2011; Liu
et al., 2015).
Malachite green and formalin are the most potent anti-oomycete
agents although they have acute effects on aquatic ecosystems
(Schreier et al., 1996) and are teratogenic (Meyer & Jorgenson, 1983)
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10 of 22 LINDHOLM-LEHTO and PYLKKÖ
and immunosuppressive for fish if used repeatedly (Hussein et al.,
2002; Prost & Sopinska, 1989). Restrictions in the use of these
chemicals have led to a search for an effective new treatment.
Various treatments have been used to control saprolegniosis, such
as hydrogen peroxide (Ali et al., 2019; Kitancharoen et al., 1997), for-
malin (Bly et al., 1996), Bronopol (Pyceze), NaCl, acetic acid, povidone
iodine (Fuangsawat et al., 2011), ozone, UV (Rahkonen & Koski, 2002),
KMnO4 (Sherif & Abdel-Hakim, 2016), NaOCl (Khomvilai et al., 2005),
ClO2 (Prasatporn et al., 2010), chitosan (Min et al., 1994), triclosan
(Kumar et al., 2020) and copper fibres (Emara et al., 2020; Miura et al.,
2005). They have all shown lower efficiency than malachite green
(Bruno et al., 2011; Liu et al., 2015) which was banned in 2002 (due to
toxicity, Fernandez et al., 1991). Many include safety concerns, caus-
ticity can cause tissue damage (Burka et al., 1997), or their application
in large volumes of water is impractical (Branson, 2002; Oono et al.,
2008). They can even change the biological properties of water and
contaminate the environment (Battaglin & Fairchild, 2002; Özçelik
et al., 2020). Additionally, probiotics (Lategan et al., 2004) and biologi-
cal control agents havebeen studied, suchasPythium (Hussein&Hatai,
2002) and Aeromonas (Lategan et al., 2004; Sherif & Abdel-Hakim,
2016), but they also have limitations. Vaccination against saprolegnio-
sis has also been proposed, but its application is costly and impractical
(Fregeneda-Grandes &Olesen, 2007;Minor et al., 2014).
Bronopol (2-bromo-2-nitropropane-1,3-diol) and its methyl deriva-
tive (2-methyl-4-isothiazolin-3-one) oxidize thiol groups of protein and
inhibit dehydrogenases. They have been considered promising for the
control of Saprolegnia spp. (Oono &Hatai, 2007). However, some of the
Saprolegnia strains are tolerant for bronopol (Rezinciuc et al., 2014).
Hydrogen peroxide, sodium percarbonate and peracetic acid are
used for bathing infected fish and kill various parasites (Bruzio & Buch-
mann, 2010; Meinelt et al., 2009). Hydrogen peroxide appears to be a
promising chemical for the treatment of Saprolegnia spp. (Fitzpatrick
et al., 1995; Marking et al., 1994) with minimal impact on the envi-
ronment (Mitchell & Collins, 1997). For example, it has been useful in
treating infections in catfish (Howe et al., 1999). However, it can induce
adverse side effects such as reduced fish growth and damage to the
gills (Mustafa, 2019), and the species, life stage andwater temperature
should be considered when treating Saprolegnia spp. with hydrogen
peroxide (Rach et al., 1997). Hydrogen peroxide appears an effective
anti-oomycete agent in trout eggs (Lovetro, 1998; Rach et al., 1997);
but in many cases, it is accepted only as a disinfectant.
KMnO4 has been tested and found to be an effective anti-oomycete
agent in eggs of several species. Zahran and Risha (2013) reported
that KMnO4 had a beneficial effect against saprolegniosis and showed
a protective role against oxidative damage in saprolegniosis-infected
Nile tilapia. Das et al. (2012) suggested that at the beginning of Sapro-
legnia infection, fish should be treated in two steps: dip treatment with
4 g salt per litre of water for 2 min, followed by 5 ppm KMnO4 for
10min, resulting in faster recovery.
Peracetic acid has proven activity against S. parasitica but it causes
lacrimation and irritation to the upper respiratory tract in humans
(Marchand et al., 2012). Boric acid inhibits the germination and col-
onization of spores and mycelial growth (Ali et al., 2014) but excess
amounts affect DNA integrity and reduce fish growth (Öz et al., 2018).
Among the current treatments, the least harmful is NaCl, but it is effec-
tive only in high concentrations which prevents its use in freshwater
systems (Das et al., 2012).
The tolerance of Saprolegnia spp. to high salinity has thus far been
inadequately studied (Ali, 2005). Salt dips release osmotic stress in
fish, affectingwatermould infection (Straus et al., 2009; Treves-Brown,
2000). In previous studies, seawater at 29 g L−1 and salt water (NaCl
solution) at 15 g L−1 were lethal to Saprolegnia spp. (Marking et al.,
1994; Pickering, 1994) and effective for controlling saprolegniosis
(Willoughby, 1994).
Ali (2005) reported that the vegetative growth of S. parasitica
decreased as the concentration of NaCl increased and the vegeta-
tive hyphae were branched and crippled at 0.07 and 0.10 M. The
synergistic action of salinity and ascorbic acid significantly enhanced
sporangial production and to some extent, sporangial release at var-
ious concentrations compared to salinity alone. Only the two highest
concentrations of NaCl supplied with 5.68 mM ascorbic acid inhibited
sporangial formation (Ali, 2005). The different concentrations of NaCl
and ascorbic acid significantly promoted the cellulolytic activity of S.
parasitica at low and moderate concentrations but inhibited it at high
concentrations. The growth of S. parasitica declined as concentrations
of NaCl and ascorbic acid increased until 0.14M.
Ascorbic acid affected both sporangia formation and release to a
lesser extent than NaCl, which was gradually inhibited by increasing
the salt level up to 3.41mM (Ali, 2005). Low concentrations of ascorbic
acid had no effect on the formation of reproductive organs, whereas
moderate concentration affected their number, and morphogenesis
and high levels completely inhibited their formation (Ali, 2005). These
findings are promising for finding an efficient and non-toxic treatment.
Ozone is considered relatively safe and poses no risk to the envi-
ronment due to its short half-life. The complete elimination of certain
bacteria (Aeromonas salmonicida, Vibrio anguillarum, Vibrio salmonicida
and Yersinia ruckeri) has been observed (Liltved et al., 1995). The use
of ozone requires particular care in adult fish, and it leads to death,
even at low concentrations (Forneris et al., 2003). Forneris et al. (2003)
studied the effects of O3 at 0.01; 0.03; and 0.2 mg L
−1 for 10 min daily
and compared themwith similar formaldehyde treatments to treat fish
eggs. They reported similar efficiency with both compounds, but the
0.3mgO3 L
−1 dose was above the toxicity threshold.
Many studies have been performed on various inorganic substances
and heavy metals (Jung et al., 1999; Yeo et al., 1995) which have wide
antibacterial properties (Cho et al., 2005). For example, silver, copper,
zinc and other metals bound to inorganic carriers are more efficient
than inorganic disinfectants. Various silver-containing antibacterial
and antifungal materials have recently been developed (Shahverdi
et al., 2007; Shokouh Saljoghi et al., 2020; Wang et al., 2007; Xu et al.,
2011), and some are in commercial use. Silver has a wide antibacterial
spectrum, and it is relatively safe to use (Cho et al., 2005). For example,
Shokouh Saljoghi et al. (2020) used nano-silver zeolite (SZ) and ben-
tonite on fish pathogens and in in vitro experiments and studied their
effect on Saprolegnia spp. They concluded that nano-SZ and bentonite
had antifungal activities and potential candidates for indirect use in
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LINDHOLM-LEHTO and PYLKKÖ 11 of 22
aquaculture. Additionally, SZ and silver nanoparticles have been found
efficient against Saprolegnia spp. at 600 mg L−1 concentration (Johari
et al., 2014) and even to increase the hatchability of eggs and larval
survival (Soltani et al., 2010).
Silver, copper, zinc and other metals can be bound to inorganic
carriers for slow release and act better as disinfectants compared to
conventional organic options (Bailey, 1983; Johari et al., 2014). Inor-
ganic carriers include zeolite, apatite, phosphates, titanium dioxides
and glass. Zeolite is a porous material of hydrated sodium aluminosil-
icate, showing a strong affinity with silver ions, and it can electrostat-
ically bind up to 40% (w/w) (Uchida, 1995). SZ has been the subject of
studies for medicine and the hygiene industry (Morishita et al., 1998;
Nikawa et al., 1997).
Silver ions affect DNA molecules, causing a loss of the replication
abilities of DNA, and interact with thiol groups in protein, inactivat-
ing the bacterial proteins. For example, Feng et al. (2000) investigated
the inhibitionmechanism of silver ions onmicroorganisms. Johari et al.
(2014) studied the antifungal activity of SZ and determined the min-
imum inhibitory concentrations. They used powdered SZ in glucose
yeast extract, and the growth of Saprolegnia spp. on the SZ agar was
compared to SZ-free agar. The results showed that SZ inhibited the
growth of Saprolegnia spp. The minimum inhibitory concentration for
Saprolegnia spp. was at 600 mg L−1. This showed that SZ was a good
candidate to replace other toxic antifungal agents. However, the study
of Johari et al. (2014) needs to be repeated at lower temperatures (i.e.,
10–12◦C) to understand the inhibitory effects of SZ and its potential
use in systems for cold water fish species.
Mixing approximately 0.06% SZ into the structure of aquaculture
equipment seemed to minimize Saprolegnia spp. growth (Johari et al.,
2014). It is now necessary to find the best applicable methods to use
SZ in aquaculture systems, such as fishponds, hatcheries and aquari-
ums. For example, SZ can be incorporated into the filter media used in
the water filtration systems of recirculation systems and hatcheries to
control bacterial and fungal diseases transmitted and spread through
water (Johari et al., 2014). On the other hand, SZ can be included
in the polymeric structures of aquaculture systems such as fibre-
glass or polyethylene troughs, trays, culture tanks and other rearing
instruments as an antimicrobial and antifouling agent (Johari et al.,
2014).
Copper nanoparticles are used in many applications in agricul-
ture, livestock, medicine and many other areas (Borkow & Gabbay,
2009; Kalatehjari et al., 2015). Copper and copper-based compounds
are known to remove a wide range of yeasts and fungi (Belli et al.,
2006; Zatcoff et al., 2008), but their antifungal properties depend on
concentration (Cioffi et al., 2004).
Kalatehjari et al. (2015) studied if copper nanoparticles could act
against S. parasitica. They measured the minimum lethal concentra-
tion of copper nanoparticles on Saprolegnia sp. in yeast extract glucose
chloramphenicol agar. They observed that copper nanoparticles from
10 ppm had antifungal effects on Saprolegnia sp. The antifungal effects
of copper nanoparticles were positively correlated with both concen-
tration and time of exposure.
Certain antibiotics have been studied to treat Red Skin Disease
and Saprolegnia infections (Toranzo et al., 2005; Xi et al., 2019). For
example, oxytetracycline and sulfadiazine have been administered to
bighead carp during breeding (He et al., 2016; Toranzo et al., 2005;
Xi et al., 2019). Antibiotics were already tested in 1978, when Oláh
and Farkas (1978) studied the effects of 33 antibiotics against Sapro-
legnia spp. and Achlya spp. They observed significant inhibiting effects
only for nalidixic acid against Saprolegnia spp. More recently, pen-
tacyclic indolosesquiterpenes (Oridamycins A and B) were studied
and showed antiparasitic activity against S. parasitica at 3.0 μg mL−1
(Takada et al., 2010). Additionally, two angucycline compounds related
to saquayamycin antibiotics were found effective (Saprolmycin A 3.9
and E 7.8 ng mL−1) as anti-saprolegniosis candidates (Nakagawa et al.,
2012). However, a suitable antibiotic against saprolegniosis is not
commercially available.
4.3 Plant-based treatments
Plant extracts are known to play an essential role in several biological
activities. Several plant extracts can improve fish growth and immunity
or cure diseases. Certain plants and plant extracts contain significant
amounts of antifungal and antibacterial compounds with medicinal
properties (Milutinović et al., 2021; Shah et al., 2021). For example,
pomegranate extracts, clove and Thymus linearis have been proposed
as potential treatments for saprolegniosis (Shah et al., 2021).
Various herbs have been utilized in their crude or extracted forms
to stimulate fish immune systems (Table 2). These include onion (Allium
cepa) and garlic (Allium sativum), which have been used medicinally
since ancient times (Núñez-Torres et al., 2022; Özçelik et al., 2020) and
contain various bioactive compounds such as organosulfurs, flavonols,
ascorbic acids and carbohydrate prebiotics. These compounds have
anti-inflammatory, antimicrobial, antioxidative, antistress, anticancer
and immunomodulatory effects (Sagar et al., 2022). Furthermore, the
phenolic compounds and fatty acids of plant extracts have shown
antimicrobial activities (Maftuch Kurniawati et al., 2016; Puupponen-
Pimiä et al., 2001; Stanković et al., 2012).
Various organophosphates have been tested in aquaculture. Con-
centrations as low as below 1 mg L−1 are known to limit infections
(Kabata, 1985). Even pyrethroids have been used as a parasiticide
(Kabata, 1985). They are extracts of the plant Chrysanthemum. How-
ever, pyrethroids are toxic to fish, and their application requires caution
(Bakke et al., 2018).
The essential oils of Eryngium campestre, Mentha piperita and
Cuminum cyminum have shown antifungal activity against S. parasit-
ica (Adel et al., 2020). The major constituents in the studied essential
oils were bornyl acetate (17.9%) in E. campestre, menthol (48.5%) inM.
piperita and α-pinene (29.1%) in C. cyminum. Adel et al. (2020) reported
minimum fungicidal concentrations of 0.5 μg mL−1 for C. cyminum and
1 μg mL−1 for M. piperita and E. campestre. The results suggest that
the essential oils may be potential plant-based antifungal components
against S. parasitica.
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12 of 22 LINDHOLM-LEHTO and PYLKKÖ
TABLE 2 Examples of plant-based treatments, concentrations and effects in treating saprolegniosis with references.
Treatment Concentration Effects for fish/inhibition Reference
Essential oils of Eryngium
campestre,Mentha piperita,
Cuminum cyminum
0.5 μgmL−1 for Cuminum
cyminum
1 μgmL−1 forMentha piperita and
Eryngium campestre
Zone of inhibition C. cyminum 27.4mm;M.
piperita 22.6mm; E. campestre 24.8mm
Adel et al. (2020)
Extracts of Cyperus esculentus
and Carthamus tinctorius
0.1mg L−1 >80% and 70% inhibition against Saprolegnia
parasitica
Emara et al. (2020)
Solution of catappa leaf
(Terminalia catappa)
500mg L−1 59% survival rate of juvenile gourami
(Osphronemus goramy) infectedwith Saprolegnia
sp.
Grandiosa et al. (2022)
ThymoquinoneNigella sativa oil 4 μgmL−1 in 160 μgmL−1 for
30min
Zoospores of S. parasitica could not germinate Hussein et al. (2002)
Extract of garlic Allium sativum 500mg L−1 20min d−1 Absence of fungal structures of cotton specks
39% and depigmentation 33.5%
Núñez-Torres et al. (2022)
Pennyroyal+Myrtus communis,
Thymus daenensis essence oils
5 μLmL−1 + 10 μLmL−1 The best antifungal effect for rainbow trout
(Oncorhynchus mykiss) eggs against S. parasitica
Salehi et al. (2015)
Ethanolic extract of Thymus
linearis
0.32mgmL−1
5.12mgmL−1
Hyphal growth inhibition 54.5%± 0.9%
100% inhibition against S. parasitica
Shah et al. (2021)
In previous years, anti-oomycetes activities of some plant extracts
Ceramium rubrum, Magnolia officinalis and Zingiber officinale have been
observed (Caruanaet al., 2012;Huanget al., 2015). Themedicinal prop-
erties of the genus Thymus L. have long been known (Chraibi et al.,
2016; Javed et al., 2013). For example, T. linearis has antibacterial
(Gilani et al., 2010), anti-cancer (Hussain et al., 2012) and anti-viral
properties (Hafidh et al., 2009). Shah et al. (2021) assessed a plant
extract of T. linearis to evaluate anti-oomycetes activity against S. par-
asitica. T. linearis extract was able to reduce hyphal growth by 54.45%
at 0.32 mg mL−1 and 100% at 5.12 mg mL−1, leading to a complete
reduction of zoospore production.
Emara et al. (2020) studied 59 plants or plant parts and screened
for possible antifungal properties against S. parasitica. They found
eight plant extracts in which Cyperus esculentus induced the highest
inhibition rate. C. esculentus and Carthamus tinctorius extracts were
the most effective at a concentration of 0.1 mg L−1. Additionally,
methanolic extracts of C. esculentus, Chenopodium murale plant, C. tinc-
torius flowers, Ipomoea batatas leaves, Juniperus phoenicea fruits, Luffa
aegyptiaca leaves and fruit rend, and Ricinus communis leaves showed
high inhibitory action against Saprolegnia spp. at low concentrations.
They should be studied in more detail to assess their potential for
aquaculture applications against saprolegniosis.
Catappa leaf plant (Terminalia catappa) has antifungal properties
(Caruso et al., 2013). Previously, catappa leaves have been stud-
ied, focusing on fish infected with Aeromonas hydrophila bacteria or
treating Saprolegnia sp. on fish eggs (Yakubu et al., 2020). Later,
Grandiosa et al. (2022) studied if catappa leaf solution was suit-
able in treating juvenile gourami infected with Saprolegnia sp. They
used doses of 500, 1000, 1500 and 2000 mg L−1 to prevent any
harmful side-effects or toxicity. They observed that the growth of
Saprolegnia sp. was reduced (Grandiosa et al., 2022), and the highest
survival rate of juvenile gourami was found in treatment with 500 ppm
(59%). This is presumably due to the phytochemicals in catappa leaf,
which function as antimicrobials. Catappa leaf contains flavonoids,
saponins, triterpenes, diterpenes, phenolic compounds and tannins
(Pauly, 2001). However, although the treatment increased the survival
of gourami, catappa leaf treatment could not fully remove infections of
Saprolegnia.
Thus far, suitable compounds have been sought among plant
extracts with fungicidal properties (Rai et al., 2002), and essential
oils (Madhuri et al., 2012; Tampieri et al., 2003). Salehi et al. (2015)
demonstrated that Eucalyptus globulus, Thymus daenensis and forty
other essential oils were effective in suppressing the fungal growth
of S. parasitica. The best results were observed with T. daenensis and
Myrtus communis essence oils in the presence of pennyroyal essence
oil.
Mostafa et al. (2020) studied the antifungal potency of the plant
extracts of Nigella sativa, Punica granatum, Thymus vulgaris and Z.
officinale against saprolegniosis. Their results showed that two plant
extracts provided a significant inhibition of mycelial growth of the
pathogenic Saprolegnia diclina isolate. P. granatum extract showed a
potential suppressive effect on the growth parameter of S. diclina at
a concentration of 0.5 mg mL−1, followed by extract of T. vulgaris,
whereas the other plant extracts had no suppressive potency at the
same concentration.
N. sativa (black cumin) is an herbaceous plant which grows annually
in countries near the Mediterranean Sea. Its seeds have tradition-
ally been used for medicinal purposes. Hussein et al. (2002) studied
the antimycotic activity of thymoquinone (2-isopropyl-5-methyl-1,
4-benzoquinone), a major carbonaceous component of N. sativa oil
against water mould. N. sativa oil had a fungicidal effect and inhib-
ited the growth of water mould at a concentration of 160 μg mL−1.
The zoospores of S. parasitica could not germinate after exposure to
4 μg mL−1 thymoquinone for 30 min (Hussein et al., 2002). However,
thymoquinone is toxic to salmonids and cyprinids, suggesting that its
toxicity against other fish species should be tested.
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LINDHOLM-LEHTO and PYLKKÖ 13 of 22
5 CONCLUSIONS
The factors influencing Saprolegnia infections in the environment and
on fish farms are still largely uncertain. Stressors such as malnu-
trition, crowding, stress, temperature shocks, or unsuitable water
temperature, spawning, poor water quality, injuries from handling and
high fish density have been associated with outbreaks. For exam-
ple, water temperature and changes of temperature, a high organic
load, nitrogen compounds, salinity, conductivity, the content of Ca2+
ions and microorganisms seem to be connected with saprolegniosis
occurrences. However, it is unclearwhy some farms have frequent out-
breaks, whereas others remain disease-free. In the future, connections
among different water quality parameters with saprolegniosis occur-
rences need to be systematically and scientifically studied. For fish
farmers, this could act as warning signs for saprolegniosis and as a
signal for starting a treatment.
For long, malachite green was the most effective treatment against
saprolegniosis. It was banned in edible fish world-wide in 2002 due to
its carcinogenic and toxic effects. This has forced farmers to use alter-
native disinfection methods against Saprolegnia spp. Many compounds
have since been tested and studied, but a suitable and safe compound
to treat saprolegniosis remains to be found. Formalin, an aqueous solu-
tion of 37% formaldehyde, is widely used, but it is not efficient enough
to sufficiently control fungal infections in fish and eggs. Other treat-
ments have been used to control saprolegniosis, such as Bronopol
(Pyceze), salt (NaCl), acetic acid, povidone iodine, ozone, hydrogen per-
oxide, UV, potassium permanganate, sodium hypochlorite and chlorine
dioxide, to name only a few. Many include safety concerns, their caus-
ticity can cause tissue damage to reared species, or their application in
large volumes of water is impractical. It is of high importance to find an
effective and non-toxic treatment agent, and research efforts should
bemade to achieve this goal.
Certain plants and plant extracts contain significant amounts of
antifungal and antibacterial compounds. Various plant-based com-
pounds, such as phenolic compounds, fatty acids, organosulphates and
pyrethroids, have been tested in aquaculture against Saprolegnia spp.
and other fungal diseases. For example, these can be found in onion (A.
cepa), garlic (A. sativum), extracts of Chrysanthemum, C. rubrum,M. offi-
cianalis and Z. officianalis, and essential oils of E. campestre, M. piperita,
C. cyminum and T. linearis. However, more research is required before a
suitable compound and method for large-scale rearing conditions are
established.
In aquaculture, there is an urgent need for a new and effective
treatment agent without harmful side-effects to the reared species,
environment or farming personnel. It is possible that a suitable treat-
ment can even be found among the plant-based compounds. Several
compounds and combinations havebeen tested, but further studies are
still required to attain this goal. Before an effective treatment is avail-
able in commercial use, better understanding regarding the affecting
factors is required to prevent occurrences of saprolegniosis.
AUTHOR CONTRIBUTIONS
Petra Camilla Lindholm-Lehto: Conceptualization; data curation;
project administration; writing—original draft. Päivi Pylkkö: Funding
acquisition; writing—review and editing.
ACKNOWLEDGEMENTS
Financial support provided by Natural Resources Institute Finland
(Luke) is gratefully acknowledged.
CONFLICT OF INTEREST STATEMENT
The authors declare that they have no conflicts of interest.
FUNDING INFORMATION
Natural Resources Institute Finland (Luke)
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the
corresponding author upon reasonable request.
ETHICS STATEMENT
Not applicable.
ORCID
PetraCamilla Lindholm-Lehto https://orcid.org/0000-0003-1807-
8116
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How to cite this article: Lindholm-Lehto, P.C. & Pylkkö, P.
(2024) Saprolegniosis in aquaculture and how to control it?.
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