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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
International Common Names
- English: freshwater ich; ich; ich, freshwater; Ichthyophthirus multifiliis infection of fish; ick; white spot; white spot disease of freshwater fish; white spots; whitespot; whitespots
Local Common Names
- Germany: Pünktchenkrankheit
OverviewTop of page
The phylum Ciliophora currently contains 7200 known species, but there are probably several thousand more that are as yet undiscovered (Corliss, 1979). Ciliates are found in virtually all bodies of water, ranging from small ponds or streams to open oceans. Most are free-living, but many occur as commensals or symbionts, and a few are parasites of invertebrates and vertebrates. Ciliates range in size from approximately 10 µm to 4500 µm and their body shape varies from nearly spherical to highly ovoid (Corliss, 1979). They have a rigid body form, resulting from a distinct fibrous cortex just below the surface plasma membrane. The ciliate cell has a large number of organelles and inclusions. Some distinguishing characteristics of ciliates are listed below (Corliss, 1979; Nanney, 1980):
- Nuclear dimorphism. With few exceptions ciliates possess two nuclei, a transcriptionally active macronucleus and at least one germ-line micronucleus.
- Cilia or compound ciliary organelles, such as cirri. These are often present in large numbers and arranged in distinct patterns. Some species have them only in one stage of the life cycle.
- Infraciliature located below the surface of the cell. This infrastructure consists of basal bodies and a host of more or less closely associated microtubules and fibrils.
- A cytostome, or cell mouth, is usually present.
Some ciliates are commensals on the gills or skin of fishes and others (such as Tetrahymena spp.) are opportunistic parasites. Ciliates are often found on dead or moribund fishes. Parasitic ciliates are not common.
I. multifiliis, Fouquet, 1876 is a pathogenic ciliate that infects freshwater fishes.
I. multifiliis, also referred to as Ich, is one of the most pathogenic protozoan parasites of fishes. There is no official record on the annual economic loss attributed to ichthyophthiriasis, even though it is considered to be a major problem in aquaculture (Hoffman, 1999). Epizootics were reported in China as early as the 10th century (Hines and Spira, 1974a). The first major outbreak in North America was described at the end of the 19th century (Stiles, 1894). Ich was relatively unknown in Russia before 1940, but since then it has become a serious disease of carp (Bauer, 1953). The significance of the problem will increase with the growth of aquaculture.
Ichthyophthiriasis is a significant disease in fish culturing systems. Outbreaks produce financial losses, resulting not only from fish mortalities, but also from the cost of control measures and treatments. There are a variety of treatments or combinations of treatments available, none of which is ideal. An important area of research is the development of effective prophylactic control methods to prevent catastrophic outbreaks.
When available, immunization is one of the most cost- time-effective means of preventing disease. There are significant problems hindering the development of practical vaccines against I. multifiliis, however. One of the major obstacles is that these ciliates cannot be grown in axenic culture, which precludes the large-scale culture of organisms for preparation of vaccines. Future research should address the problem of mass production of protective antigens. One solution is the development of in vitro cultivation systems for I. multifiliis, which will require basic studies on parasite physiology and biochemistry. The current and future resources provided by genomic technologies in ciliates are sure to provide advances in this area. The genome of the free-living ciliate T. thermophila is currently available for comparative studies (Turkewitz et al., 2002), and an Ichthyophthirius expression sequence tag library is under construction (T.G. Clark, unpublished). A second solution would be the use of genetic engineering for the production of recombinant protective antigens in easily cultured organisms. The free-living ciliate T. thermophila is a promising system for the large-scale production of heterologous genes, and has already been successfully used to express the i-antigens of I. multifiliis (Gaertig et al., 1999).
Further research is also necessary to understand the immune response against this parasite. Although it has been evident for some time that fishes develop protective immunity against I. multifiliis, the effector mechanisms are only now becoming elucidated. It is necessary to study further these responses in order to take logical approaches to vaccination. For example, the common antigens responsible for cross-protection among different serotypic strains of I. multifiliis remain to be characterized. Also, the pathways through which antigens are presented and processed at mucosal surfaces remain to be determined. Likewise, the mechanisms of antibody production and transport to mucosal surfaces require further study.
Methods to preserve and maintain infective organisms are needed. One of the problems in immunization trials is the lack of standard challenge methods. If viable parasites could be preserved by freezing, then standard isolates would be available for these purposes. Preservation techniques would benefit other areas of research as well. Collection and cryopreservation of isolates from different geographical areas, with different fish species and at different times would allow comparative studies. This could help to resolve taxonomic questions related to number of species of Ichthyophthirius. Also, the question of biotypes or strains and host specificity could be investigated in more detail.
[Derived from: Woo, PTK, ed., 2006. Fish diseases and disorders, Volume 1: Protozoan and Metazoan infections. (2nd edition) Wallingford, UK: CAB International]
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Acipenser baerii baerii (siberian sturgeon)||Domesticated host, Wild host||Aquatic: All Stages||Enclosed systems/Freshwater recirculating systems|Enclosed systems/Ponds|Enclosed systems/Raceways / running water ponds|Enclosed systems/Tanks|
|Anguilla japonica (Japanese eel)||Domesticated host, Wild host||Aquatic: Adult|Aquatic/Fry||Enclosed systems/Ponds|
|Aristichthys nobilis (bighead carp)||Aquatic: Adult|Aquatic/Fry||Enclosed systems/Ponds|Enclosed systems/Tanks|
|Betta splendens (Siamese fighting fish)||Aquatic: Adult|Aquatic/Fry||Enclosed systems/Aquaria (marine / freshwater ornamentals)|
|Bidyanus bidyanus (silver perch)||Aquatic: Adult||Enclosed systems/Ponds|
|Carassius auratus auratus (goldfish)||Domesticated host||Aquatic: Adult|Aquatic/Broodstock|Aquatic/Fry||Enclosed systems/Aquaria (marine / freshwater ornamentals)|Enclosed systems/Ponds|
|Cichlasoma urophthalmum (Mayan cichlid)||Aquatic: Adult|Aquatic/Fry||Enclosed systems/Tanks|
|Colossoma macropomum (tambaqui)||Domesticated host, Wild host||Aquatic: Adult|Aquatic/Broodstock|Aquatic/Larval|Aquatic/Fry||Enclosed systems/Aquaria (marine / freshwater ornamentals)|Enclosed systems/Cages|Enclosed systems/Freshwater recirculating systems|Enclosed systems/Other enclosed systems|Enclosed systems/Ponds|Enclosed systems/Tanks|
|Ctenopharyngodon idella (grass carp)||Aquatic: All Stages||Enclosed systems/Ponds|Enclosed systems/Tanks|
|Cyprinus carpio (common carp)||Domesticated host, Wild host||Aquatic: Adult|Aquatic/Broodstock|Aquatic/Fry||Enclosed systems/Ponds|
|Dorosoma cepedianum||Wild host|
|Fundulus notatus||Wild host|
|Helostoma temminckii (kissing gourami)||Aquatic: All Stages||Enclosed systems/Aquaria (marine / freshwater ornamentals)|Enclosed systems/Cages|Open water systems/Enhancements and culture-based fisheries (inc. ranching and stock enhacement)|Enclosed systems/Pens|Enclosed systems/Ponds|Enclosed systems/Ricefield aquaculture|Enclosed systems/Tanks|
|Ictalurus punctatus (channel catfish)||Domesticated host, Wild host||Aquatic: Adult|Aquatic/Broodstock|Aquatic/Larval|Aquatic/Fry|
|Micropterus dolomieu (smallmouth bass)||Wild host|
|Micropterus salmoides (largemouth bass)||Wild host|
|Oncorhynchus mykiss (rainbow trout)||Domesticated host, Wild host|
|Oncorhynchus nerka (sockeye salmon)||Wild host|
|Oncorhynchus tshawytscha (chinook salmon)||Domesticated host, Wild host||Aquatic: Adult|Aquatic/Fry|
|Oreochromis aureus (blue tilapia)||Wild host|
|Paralichthys olivaceus (bastard halibut)|
|Perca flavescens (yellow perch)||Wild host|
|Poecilia reticulata (guppy)||Wild host|
|Salmo salar (Atlantic salmon)||Domesticated host||Aquatic: Adult||Enclosed systems/Ponds|
|Salmo trutta (sea trout)||Domesticated host, Wild host||Aquatic: Adult|
|Xiphophorus maculatus (southern platyfish)||Wild host|
Hosts/Species AffectedTop of page
Ich appears to parasitize all freshwater fishes. There are no records of species with complete natural resistance (Ventura and Paperna, 1985). There are suggestions of variation in the degree of susceptibility between fishes, however. These variations may depend on such factors as genetic background, physiological status of the fishes, parasite strains and environmental conditions (Clayton and Price, 1988, 1994).
Epizootics in native fish populations often occur in only one species of fish. Elser (1955) reported on an outbreak in a reservoir in Maryland in which the disease affected predominantly yellow perch (Perca flavescens). Allison and Kelly (1963) described an epizootic in rivers of north-western Alabama. The majority of infected fishes were gizzard shad (Dorosoma cepedianum) and threadfin shad (Dorosoma petenense). In an outbreak reported in Kentucky the only fishes infected were blackstripe topminnows (Fundulus notatus) (Kozel, 1976). An epizootic that occurred in Lake Titicaca on the Peru-Bolivia border primarily affected killifish (Orestias spp.) and the majority (93%) of dead were O. agassii (Wurtsbaugh and Tapia, 1988). The occurrence of epizootics in only one or a few species in a mixed fish population may not indicate genetic variation in resistance, but rather different physiological states that predispose certain individuals or groups to disease. Wurtsbaugh and Tapia (1988) observed that most of the fishes that died in the epizootic were gravid or spent adult O. agassii. Pickering and Christie (1980), in a study on parasite infection of brown trout (Salmo trutta L.), found Ich more frequently in precocious mature pre-spawning males than in immature fishes. They concluded that sexual maturation was associated with an increase in prevalence and severity of infestation with ectoparasites. Reproductive stress may also be a factor in the apparent variation in susceptibility to infection.
Nigrelli et al. (1976) proposed that there are physiological races of I. multifiliis related to the temperature tolerances of the host fishes. Thus, races of I. multifiliis exist that infect cold-water (7.2-10.6°C) fishes, such as salmon, and others that infect warm-water (12.8-16.1°C) tropical fishes. To date, there is no experimental evidence to substantiate or refute this idea. Fishes with wide ranges of temperature tolerance, such as carp and catfish, may be susceptible to both cold- and warm-water parasites. Ich epizootics in Arctic fishes suggest that these outbreaks occur when the water temperature reaches a moderate range. Valtonen and Keränen (1981) reported on an epizootic in a salmon hatchery in central Finland in two consecutive years when the water temperature rose to 14°C or higher.
Paperna (1980) stated that I. multifiliis in Europe and Asia is highly pathogenic for carp, with a preference for this species. There are no experimental data to support this speculation. Although ichthyophthiriasis often occurs in carp in Europe and Asia, this could merely be due to the fact that carp are the primary fish raised in these areas and intensive culture conditions predispose them to infection.
DistributionTop of page
Ich is a cosmopolitan parasite of fishes (Nigrelli et al., 1976; Valtonen and Keränen, 1981). Infections have been reported from virtually all regions where fishes are cultured, including the tropics and subarctic, as well as in feral fish populations from most continents (Nigrelli et al., 1976; Valtonen and Keränen, 1981). Fouquet first described the organism in France in 1876 (Stiles, 1894). According to Stiles, Hildendorf and Paulick published observations on a fish disease caused by a ciliate (presumably I. multifiliis) in Hamburg, Germany, in 1869. These were the first detailed descriptions of the parasite and its life cycle. The disease was known in fishes in Europe in the Middle Ages (Hoffman, 1999), however. There is evidence that it originated in Asia as a parasite of carp (Dashu and Lien-Siang, referenced by Hines and Spira, 1974a).
The worldwide spread of the parasite was facilitated by transportation of fish by humans (Nigrelli et al., 1976). Paperna (1972) reported on an outbreak in Uganda and noted that I. multifiliis was not found in that country in a previous study. He further indicated that a number of fish species had been imported into Uganda from the USA and Hong Kong. Wurtsbaugh and Tapia (1988) described an epidemic in fishes in Lake Titicaca on the Peru-Bolivian border. They noted that a number of fishes, salmonids and atherineds, had been introduced into Lake Titicaca and its watersheds at various times in the past.
Bragg (1991) found a higher incidence of Ich in salmonid fishes from South African rivers in areas where intensive aquaculture occurred. He suggested that aquaculture contributed to increased infections in both river and hatchery fishes. In contrast, epizootics of Ich occurred in adult sockeye salmon, Oncoryhynchus nerka, during the 1994 and 1995 spawning seasons in the Skeena River watershed in northern British Columbia, Canada. In this case, it is suggested that resident fish were the most likely source of the parasite in the watershed because several species were found with light infections of Ich. Transmission of the parasite to anadromous sockeye salmon was probably enhanced by the high density of fish held below the spawning grounds prior to moving into the spawning area (Traxler et al., 1998).
Distribution TableTop of page
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|South Africa||Present||Bragg (1991)|
|China||Present||Hines and Spira (1974)|
|Finland||Present||Valtonen and Keranen (1981)|
|Canada||Present||CABI (Undated)||Present based on regional distribution.|
|-British Columbia||Present||Traxler et al. (1998)|
|United States||Present||CABI (Undated)||Present based on regional distribution.|
|-Alabama||Present||Allison and Kelly (1963)|
|Bolivia||Present||Wurtsbaugh and Tapia (1988)|
|Peru||Present||Wurtsbaugh and Tapia (1988)|
PathologyTop of page
Ichthyophthirius multifiliis does not appear to have a predilection for any specific group of fishes, although it is believed that the organism originated as a parasite of carp (Hoffman, 1999).
There is a linear relationship between the number of theronts to which a host is exposed and the resultant parasite burden (McCallum, 1982). Theronts are positively phototactic (Lom and Cerkasova, 1974; Wahli et al., 1991). Wahli (1991) could not demonstrate that theronts were attracted to fish, a result in disagreement with that of Lom and Cerkasova (1974), who found that theronts were attracted by components of fish blood. Houghton (1987) observed that theronts were attracted to pieces of fish tissue in the water, suggesting a possible short-range homing mechanism.
Epizootics of I. multifiliis appear to occur uniformly in populations of male and female fishes. There are reports where infections occurred predominantly in one sex, however. Male guppies (Lebistes reticulatus) were reported to be more severely infected than females (Paperna, 1972). Similarly, in brown trout (S. trutta) mature males were more frequently infected than females, with the most severe infections occurring on precociously mature pre-spawning males (Pickering and Christie, 1980). In contrast, in an epizootic in Lake Titicaca, the majority of the dead and infected fish were gravid or spent female killifish (O. agassii) (Wurtsbaugh and Tapia, 1988). Infection may not be a function of predilection of the parasite for either sex, but rather due to the fact that infection occurs on fishes under the greatest stress. Reproductive activity is a significant stress on fishes.
Fishes exposed to I. multifiliis can develop protective immunity (Hines and Spira, 1974c; Burkart et al., 1990); hence survivors of an epizootic are resistant to subsequent infection. Therefore, in native populations, young fishes might be more susceptible to infection than older individuals if the latter were previously exposed to the parasite. In naive feral fish populations, all ages appear to be equally susceptible to infection.
Distribution of parasite on host
Except in very severe infections, I. multifiliis is not usually uniformly distributed on the body of the fish. The parasite occurs most frequently on the dorsal surface, particularly the head and fins (Hines and Spira, 1973a; Kozel, 1976).
The gills are important sites of infection. The volume of water passing through the gills increases the opportunity for attachment, and parasites interfere with gaseous exchange once infection is established. In unstressed fishes there is very little mucus covering the secondary lamella of the gills (Handy and Eddy, 1991), which may render the gills more susceptible to infection than other body sites.
In experimental I. multifiliis infections, only a portion of the infecting theronts develop into trophonts (McCallum, 1982). McCallum (1982) suggested that this variability depends on the genetic background of the host. A major host resistance factor is the production of surface mucus, which is increased in response to infection (Hines and Spira, 1974c; Ventura and Paperna, 1985). There may be genetic factors that influence the amount and composition of fish mucus.
Significant variation in susceptibility to infection occurs among fish species. When effects due to other variables (such as time of infection and temperature) are removed, heterosis (hybrid vigor) contributes to resistance to I. multifiliis (Clayton and Price, 1992, 1994).
I. multifiliis is believed to have originated as a parasite of carp (Hoffman, 1999). The long host-parasite association may have led to the development of resistant strains of carp. Preliminary studies using scale patterns as genetic markers suggested that strains of carp vary in their resistance to I. multifiliis (Clayton and Price, 1988).
In the early stages of disease, fishes congregate near water intakes to reduce contact with free-swimming theronts (Kabata, 1985). Fishes also 'flash' or rub their bodies against objects in reaction to skin and gill irritation caused by the theronts (Brown and Gratzek, 1980). Fishes swim more rapidly than normal and often leap out of the water. As the disease progresses, they become less active and congregate at the bottom of ponds or aquaria (Hines and Spira, 1973a). Fishes also lie near the edges of ponds, moving their gill opercula rapidly in an attempt to obtain more oxygen (Kabata, 1985). This is related to gill damage caused by the parasite. With very heavy infections, fishes become lethargic and stop feeding (Hines and Spira, 1973a).
In very mild I. multifiliis infections the only detectable pathological change is the presence of a few white spots on the surface of the fishes. In more severe cases there are usually large numbers of spots on the skin (see Figs 3 and 4). Occasionally, however, I. multifiliis only infects the gills, with no obvious gross lesions on the body surface.
Ulcers develop in the skin of heavily infected fishes and are often sites of secondary bacterial or fungal infections. The fins become frayed due to loss of tissue between the fin rays (Hines and Spira, 1973a).
As mentioned earlier, mucus production is increased. Heavily infected carp have a thick, lumpy covering of surface mucus (Hines and Spira, 1974a). Increased production of mucus is not a unique response to I. multifiliis, however, as it occurs on most fishes that are exposed to irritants or skin parasites.
Infected fishes have enlarged spleens and kidneys and pale, mottled livers. Their peritoneal cavities contain fluid (Hines and Spira, 1974a). Peritoneal fluid exudation could be a secondary effect caused by opportunistic bacterial or fungal infections and/ or anorexia of the fishes in the later stages of the infection. Enlarged gall bladders (a change associated with starved animals) were reported in moribund Ich-infected carp (Hines and Spira, 1974a).
The common clinical signs of ichthyophthiriasis are the characteristic disseminated white surface lesions ('spots'). Each spot represents a developing trophont within an epithelial capsule or vesicle (see Fig. 4). Visible parasites develop several days after the initial attachment of theronts (Hines and Spira, 1973a; Ventura and Paperna, 1985). In cases where the infection is restricted to the gills, these are not visible.
An early physiological response to infection is an increase in surface mucus production (Hines and Spira, 1973a). Skin penetration by theronts stimulates expanded numbers of mucus-secreting cells in the epidermis. These multiply not only in areas around the parasite, but throughout the epidermis (Hines and Spira, 1974a). In severe infections, mucus may stream off the posterior edges of the fins and tail.
A careful observer can detect infection before the development of surface lesions by noting changes in fish behaviour (see above). Initially, infected fishes swim more rapidly and rub themselves against objects. As the disease progresses, the fishes surface in order to reach dissolved surface oxygen. They become increasingly lethargic and eventually cease feeding.
In severe infections there is erosion of the epithelia, leading to ulcer formation and exposure of the deeper tissues to bacterial and fungal invasion. A common cause of secondary invasions is the fungus Saprolegnia spp., which appears as tufts of 'fuzz' on the skin.
The nature and severity of histopathological changes seen in I. multifiliis infections vary greatly. This variation is influenced by such host factors as stress and nutritional status. Nevertheless, parasite load is the major factor contributing to the diverse tissue changes. In general, mild infections elicit minor cellular reactions. The extensive histopathological changes reported to occur in I. multifiliis infections are only seen in severe epizootics or in experimental infections with large numbers of parasites (Ventura and Paperna, 1985).
Histopathology of the skin consequent upon mild infection
In primary I. multifiliis infections (that is, the first exposure of fish to the parasite), there is little reaction to the penetrating theronts. After approximately 40 h, most trophonts are located next to the basement membrane. The cells between the parasite and the basement membrane become hydropic, vacuolated or necrotic, with pyknotic nuclei (Ventura and Paperna, 1985). The growing trophont gradually lifts and displaces the epithelial cell layers until it lies within an epithelial capsule that extends above the skin surface (Ventura and Paperna, 1985). The epithelial layer overlying the trophont expands to cover the parasite during this growth stage. The epithelium retains its architecture of differentiated cell populations (Ventura and Paperna, 1985). Cell damage is observed only in the cellular layers in direct contact with the developing trophont. Host cell debris can be observed in the food vacuoles of the trophont and in the spaces in the epithelial capsule around the parasite. There is evidence of haemorrhage occurring in the skin as a result of parasite invasion (Chapman, 1984; Ventura and Paperna, 1985). Large, pale-staining, alarm substance cells have been observed in the area of the developing trophont (Chapman, 1984). In mild infections only a few leukocytes are seen in the epithelium.
Histopathology of the skin consequent upon heavy infection
Heavy infections elicit a severe inflammatory reaction in the skin. Penetration by numerous theronts leads to increased epithelial cell hyperplasia. This cellular proliferation could be a defence mechanism (Ventura and Paperna, 1985). In addition to hyperplasia, there is a generalized increase in the number of mucus cells in the skin (Hines and Spira, 1974a). The epithelium in heavily infected fishes may be up to four times its normal thickness due to proliferation of epithelial and mucus cells (Hines and Spira, 1974a).
Extensive cell necrosis and histolysis occur around trophonts developing in the hyperplastic epithelium. Empty spaces are present, along with hydropic, vacuolated and necrotic cells (Ventura and Paperna, 1985). There is congestion in the dermal lymphatics, leading to oedema and an increased epithelial infiltration of neutrophils, eosinophils and lymphocytes (Hines and Spira, 1974a; Ventura and Paperna, 1985). The outermost epithelial cells degenerate and slough off, eventually exposing the underlying basement membrane (Hines and Spira, 1974a). It was suggested that the extensive cellular reaction observed in the skin of fishes heavily infected with I. multifiliis is a hypersensitivity reaction (Hines and Spira, 1974a; Ventura and Paperna, 1985).
Histopathology of the gills
Theronts attach to the gills at the middle or base of the gill lamellae. The young trophonts penetrate and displace the interlamellar epithelium until they reach the basement membrane (Ventura and Paperna, 1985). Host cell debris is seen in the cytoplasmic vacuoles of the parasite. Epithelial cells migrate from the apical end of the adjacent lamellae and cover the developing trophont, producing a multilayered cap over the parasite. The cell layer over the parasite also includes mucus cells and chloride cells (Hines and Spira, 1974a; Ventura and Paperna, 1985). Epithelial cell proliferation occurs not only adjacent to the parasite but also all along the lamellae (Hines and Spira, 1974a). Mature trophonts may occupy three or four lamellae (Ventura and Paperna, 1985). Mucus cells become prominent in the proliferating epithelium and comprise up to 50% of the cells in an interlamellar area (Hines and Spira, 1974a). The respiratory epithelium, however, retains its squamous morphology during this proliferation. At this time, there is a significant increase in the number of neutrophils in the area. The amount of lymphocyte infiltration is variable (Hines and Spira, 1973b). As the infection progresses, the epithelial cells continue to proliferate and eventually fill up the interlamellar space until the lamellae are completely cornified or 'clubbed' (Hines and Spira, 1974a).
In the late stages of heavy infections, complete atrophy of the gill lamella is seen, along with areas of necrosis of the gill filaments (Hines and Spira, 1974a).
Although the total leukocyte numbers do not change during I. multifiliis infections, there is a differential shift in the various leukocyte populations. Infected fishes develop a lymphocytopenia and neutrophilia (Hines and Spira, 1973a). The number of neutrophils in circulation early in the infection may increase 5-fold with no concurrent rise in total leukocyte numbers. The shift in distribution of leukocyte cell populations is accompanied by an increase in the number of immature blast cells. It was suggested that the leukocyte changes in infected fishes are non-specific stress reactions (Hines and Spira, 1973b).
Studies on serum levels of Na+, K+, Mg+ and blood urea ammonia indicated significant osmoregulatory disturbances (Hines and Spira, 1974b). In severe infections there was a marked drop in serum Na+ and Mg+ levels and a rise in serum K+ levels. Blood urea-ammonia levels also increased during the course of the infection.
It was recognized early that fishes surviving I. multifiliis outbreaks become resistant to reinfection (Bushkiel, 1910). The duration of immunity depends upon the severity of the initial infection (Bauer, 1953). A number of studies determined the period of immunity in fishes recovered from natural infections or cured by chemical treatment (Beckert and Allison, 1964; Parker, 1965; Hines and Spira, 1974c; McCallum, 1986). Immunity induced by single exposure of channel catfish to the parasite lasts for at least 3 months (Pyle, 1983). In the natural course of infection, surviving fishes eventually become free of the parasite (Valtonen and Keränen, 1981). Premunition has not been demonstrated, although a small percentage <5%) of infecting parasites developed in immunized carp (Cross and Matthews, 1992).
The immune responses of most fish are complex reactions involving the activation and interaction of a variety of cell populations and the production of humoral factors, including antibodies. Some host reactions are general, responding similarly no matter what parasite is encountered; others are specific, reacting only with the parasite that induced the reaction. The former responses are innate reactions, and the latter are referred to as adaptive or acquired. In I. multifiliis infections, both innate and adaptive reactions appear to play significant roles.
Surface mucus is the fish's first line of defence against infection. To infect, theronts must penetrate this mucus layer and burrow into the epithelium. Mucus-secreting cells increase in the skin of infected fishes (Hines and Spira, 1973a; Ventura and Paperna, 1985). Heavily parasitized fishes characteristically have a thicker mucus coat than uninfected fish. Theronts have limited energy stores, which could become depleted during penetration of the thickened mucus layers. Trapped theronts would eventually be removed from the surface with the excess mucus. In this regard, the naturally thin mucus layer of gills could be a predisposing factor for infection at this site. One report indicated that the mucus layer does not completely cover the secondary lamellae in unstressed rainbow trout (Handy and Eddy, 1991).
In addition to acting as a physical barrier, surface mucus also contains antiparasitic factors. Hines and Spira (1974c) and Wahli and Meier (1985) found that mucus and serum from immune carp and rainbow trout (Salmo gairdneri) immobilized trophonts in vitro. It was suggested that this immobilizing activity was due to the presence of antibodies and that these prevented the penetration of theronts through the mucus. Xu and Dickerson, using dot-blot assays, found that Ich-immune channel catfish have mucus antibodies against membrane antigens of I. multifiliis (Xu, 1995). In contrast, Cross and Matthews (1993a) were unable to demonstrate binding of carp mucus antibodies to thin sections of fixed theronts. The discrepancy in these findings is probably due to the fact that specific antibodies are present in relatively low levels in mucus (as compared with serum) and may not have been detectable in the experiments of Cross and Matthews. More recent work suggests that mucosal antibodies are protective. This work is discussed further below.
A basic innate host reaction to I. multifiliis is epithelial cell proliferation. In mild infections there is little reaction other than the formation of an epithelial cell capsule around the parasite itself (Ventura and Paperna, 1985). In severe or repeated infections, however, extensive epithelial cell proliferation occurs (Hines and Spira, 1974a; Ventura and Paperna, 1985). This epithelial hyperplasia could interfere with penetration of the theront. The skin of infected fishes also becomes infiltrated with neutrophils, basophils, eosinophils, eosinophilic granular cells, macrophages and lymphocytes (Ventura and Paperna, 1985; Cross and Matthews, 1993b). Increases in eosinophilic granular cells were coupled to the acquired immune response against the parasite (Cross and Matthews, 1993b). Leukocytes (granulocytes) were observed adjacent to parasite surfaces without apparent adherence. How these cells interact with the trophonts in the tissue is not well understood.
Some of the lymphocytes found in the skin of infected fishes are described as non-specific cytotoxic cells (NCC) (Graves et al., 1984). In laboratory experiments, NCC isolated from the anterior kidney of channel catfish were found to be cytotoxic against deciliated Tetrahymena pyriformis, a free-living ciliate. This activity was blocked following incubation of isolated NCC with formalin-killed I. multifiliis (Graves et al., 1984, 1985a, b). Based on these results, it was hypothesized that NCC also react with and kill immobilized I. multifiliis. It was found that the NCC were mobilized out of anterior kidneys in Ich-infected fishes and the circulating NCC had increased targetcell affinity and killing capacity (Graves et al., 1985b). Also, there is a decrease in lymphocytes in circulation in Ich-infected fishes (Hines and Spira, 1973b). Theoretically, this decrease could be attributed (at least partly) to NCC passing out of circulation into the skin to interact with immobilized theronts, although this has never been tested directly.
As described previously, sera and mucus collected from infected fishes immobilize theronts in vitro (Hines and Spira, 1974c). This phenomenon was taken as evidence that fishes produced antibodies against the parasite. Various antigens, including theronts (Burkart et al., 1990), trophonts (Areerat, 1974) and cilia (Goven et al., 1981), were used to induce fishes to produce immobilizing or agglutinating factors in their sera. Immobilization and agglutination were assumed to be the result of antibody activity. Nevertheless, in early studies, the precise character of the factors was not determined. It was subsequently demonstrated that channel catfish immune to Ich produce antibodies to ciliary antigens of the parasite (Clark et al., 1988). A strong positive correlation exists between antibody levels in the serum as determined by an ELISA test and the ability of the serum to agglutinate live I. multifiliis theronts in vitro. These results strongly support the conclusion that the serum anti-parasite activity is indeed antibody-mediated. Subsequent studies by Cross and Matthews (1993a) have also shown binding of fish serum antibodies to surface membranes of I. multifiliis.
The relationship between serum and mucus antibody levels is still under investigation (Maki and Dickerson, 2003). It was reported that a secretory form of antibody analogous to mammalian secretory antibody occurs in channel catfish (Lobb and Clem, 1981). Channel catfish are protected against I. multifiliis challenge following intraperitoneal injection of immobilizing murine monoclonal antibodies (mAbs) against I. multifiliis (Lin et al., 1996). Mouse antibody immunoglobulin G1 (IgG1) was transported from the peritoneal cavity to the surface of the fish, where it reacted with the parasite. In contrast, transfer of immune fish sera or immobilizing mouse IgM mAbs did not protect against I. multifiliis infection, suggesting that the teleost serum tetrameric antibody does not pass as readily to the surface as the monoclonal mouse IgG (Lin et al., 1996). An adaptive, protective immune response is elicited against Ich following the intraperitoneal injection of live theronts. As one might expect with a large extracellular parasite such as I. multifiliis, antibodies are important effectors of protective immunity (Cross, 1993; Matthews, 1994; Dickerson and Clark, 1998). Their mechanism of activity is just beginning to be elucidated. An early hypothesis was that antibodies immobilize theronts in the mucus layer of the skin (Hines and Spira, 1974c). Immobilization in vivo may be an indirect effect rather than a direct action of the antibodies on theront cilia. Clark et al. (1987) showed that immobilized theronts were surrounded by a mucus-like material, and suggested that antibody binding caused discharge of parasite mucocysts. The clumping of theronts was the result of their being trapped in this released substance. Cross (1993) demonstrated the binding of carp serum antibody to a gelatinous mucus-like material surrounding tomonts. He hypothesized that this material is responsible for immobilization in vitro and may form a barrier to further antibody binding. It was proposed by Ewing et al. (1985) that discharge of theront mucocysts is also a means of attachment and penetration into the epithelium. Premature discharge of mucocysts could result in theronts that are unable to infect fishes even though they have penetrated the surface mucus and come into contact with the epithelium.
To directly observe the fate of live parasites on fish, Cross and Matthews (1992) placed theronts on the tails of immune or naive carp and observed them under the microscope. They discovered that the parasites penetrated into the skin of both naive and immune fish within minutes. Theronts were unable to remain colonized on immune fish, however, and left within 2 h. The authors argued that immunity was the result of a humoral factor due to the rapidity of the response. There was no evidence of parasites being immobilized or killed in the tissue.
Fishes have subpopulations of lymphocytes similar to those that occur in mammals (Yocum et al., 1975; Lobb and Clem, 1982; Secombes et al., 1982). Blymphocytes develop into antibody-producing cells, and analogous cells are elicited in the antibody response against I. multifiliis. In mammals, T-lymphocytes are a well-characterized, diverse cell population involved in both regulation (e.g. TH1 and TH2 helper lymphocytes) and implementation (T-cytotoxic cells) of the immune response. T-cytotoxic cells react with antigens on cell surfaces and kill foreign antigen-bearing cells. The two model reactions for T-cell activity are delayed-type hypersensitivity reactions and graft rejection. Fishes have been shown experimentally to develop delayed hypersensitivity reactions and will reject heterologous scale grafts (Hildemann, 1972; Kikuchi and Egami, 1983; Tataner and Manning, 1983). It is unlikely that fishes develop either type of response against I. multifiliis. Houghton and Matthews (1986, 1990) argue for a cell-mediated effector response against I. multifiliis, based on experiments showing that corticosteroid treatment of Ich-immune carp increases their susceptibility to infection, while serum antibody levels remain high.
Mechanisms of disease
Fishes infected with small numbers of I. multifiliis show few signs of infection other than the development of white spots. Fishes tolerate a few parasites very well. As previously stated, this situation suggests that teleost fishes and I. multifiliis have had a long association, and as a result have evolved a balanced host-parasite relationship. Disease and/or deaths occur when there is a disturbance in this balanced interaction. This disruption is most frequently the result of infection with large numbers of parasites. When conditions are right (e.g. optimum temperature and sufficient number of hosts), the parasite population increases very rapidly. As a result, fishes are exposed to many parasites in a short period of time.
Infection by I. multifiliis triggers hyperplasia of gill epithelial cells. As a result the gill interlamellar spaces are reduced, which significantly limits the surface area available for oxygen interchange. Severe infections thus cause fishes to become oxygen-starved. In addition to being the primary site of oxygen uptake, the gills also function in both osmoregulation and excretion of nitrogenous wastes (Smith, 1929). Epithelial hyperplasia interferes with these functions as well. Infected carp have decreased levels of serum sodium andmagnesium and increased levels of serum potassium (Hines and Spira, 1974b). High levels of serum urea-ammonia nitrogen and nitrogenous wastes accumulate in the blood. An additional contributing factor to ionic imbalance is the interplay between nitrogenous waste excretion and ionic exchange. When NH+4 ions are excreted through the gills, Na+ ions are taken up from the water into circulation (Maetz and Garcia-Romeu, 1964). Thus, the decrease in NH+4 excretion during infection contributes to lowered serum Na+ concentrations. Increased mucus production in the gills of infected fishes interferes with osmoregulatory functions as fish mucus is relatively impermeable to water and ions (Hughes, 1970). Proliferative and degenerative changes in the skin also influence osmoregulation. The skin is a major barrier to ion loss and to water entry in fishes (Wikgren, 1953), and the subepidermal oedema and disruption of the epithelium cause ionic imbalance (Hines and Spira, 1974b). Finally, fishes with severe infections are under stress, and stress reactions have been reported to elicit serum ionic imbalances (Stanley and Colby, 1971; Wedemeyer, 1972).
Ich infections cause severe cellular reactions in the skin. Gradual desquamation, degeneration, necrosis and sloughing of the superficial epithelial cells occur in the area of the growing parasite (Ventura and Paperna, 1985). This devitalization of the skin reduces the ability of fishes to resist infections by opportunistic pathogens. These secondary infections add stress to an already badly compromized host and increase the mortalities in a population of infected fishes.
DiagnosisTop of page
Fishes infected with I. multifiliis usually develop characteristic white spots on their surface. In mild infections the parasites are not readily seen. The parasites are more difficult to see on fishes with lightly pigmented skin. In early stages of infection, large numbers of theronts can actually kill a fish before the parasite becomes visible and death is caused by massive damage to the gill epithelia.
Infected fishes often have behavioural changes caused by the irritation from parasites in the skin and gills. This behaviour is non-specific, however, and can also be associated with other bacterial, fungal and protozoan diseases.
To make a definitive diagnosis of ichthyophthiriosis it is necessary to microscopically examine tissue from a gill arch, a tail fin or the body surface. The large (200 to 800 µm) ciliated trophonts are easily seen in unstained wet mounts (x 10-40 magnification). The trophont of Ich has a distinctive horseshoe-shaped nucleus, which is a pathognomonic sign of infection. In early or very heavy infections, theronts will also be seen. They are ciliated and pyriform in shape and can easily be confused with Tetrahymena spp.
EpidemiologyTop of page
Seasonal fluctuations in infection
Outbreaks of I. multifiliis occur when conditions are favorable for rapid multiplication of the parasite. These include a suitable environment and susceptible fishes. According to McCallum (1982), fish density is not a constraint on the establishment of infection. Nevertheless, there does appear to be a requirement for a minimum number of fishes before an epizootic develops. Severe infections occur most commonly in dense populations of fishes.
A critical condition for an outbreak is water temperature. The duration of the developmental cycle of I. multifiliis is significantly influenced by temperature (MacLennan, 1937, 1942; Nigrelli et al., 1976; Noe and Dickerson, 1995). Generally, as the temperature rises (up to 25-28°C), parasite activity increases and the life cycle is completed in a shorter time than at lower temperatures. In addition, the number of tomites in each cyst varies with the temperature of the water, which reflects the number of cell divisions (Nigrelli et al., 1976).
Stress can bring about an outbreak in a fish population. Stress is a complex physiological reaction that causes the release of steroids from the adrenal glands, which in turn decreases the immune function of the host. A wide variety of factors induce stress in fishes: these include crowding, low dissolved oxygen, chemical pollutants in the water, high temperature and spawning activities.
Ichthyophthiriasis usually occurs when fishes are stressed and the water temperature is relatively warm. Epizootics arise in aquarium-reared fishes when optimum conditions for parasite development and rapid multiplication are present. The parasite reproduces when fishes are under stress from low oxygen and/or crowded conditions. Outbreaks occur in the spring as the water warms and when fishes are spawning (Elser, 1955; Allison and Kelly, 1963). This is very apparent in reports of disease in sub-Arctic areas. Ich epizootics in Finland occurred when water temperatures were above 14°C, and stopped as soon as the temperature fell (Valtonen and Keränen, 1981).
The cyclic nature of outbreaks is also influenced by the development of immunity in fish populations. It is well documented that fishes recovered from I. multifiliis infections develop protective immunity (Burkart et al., 1990; Matthews, 1994; Dickerson and Clark, 1996). Epizootics occur when there is a sufficiently large population of susceptible fishes. As the infection progresses, highly susceptible fishes die while those that are more resistant develop immunity. With time the majority of the surviving fishes become immune. As these conditions develop, the epizootic wanes and losses stop. The surviving population of fishes reproduces and with time the level of acquired disease resistance decreases, allowing another epizootic to occur under suitable conditions.
How does the parasite survive between outbreaks? Ich is an obligate parasite and as such requires susceptible hosts to propagate. There is no evidence of a resistant stage that allows survival during environmental changes or in the absence of fishes. Thus, it is most likely that the parasite is maintained through a low-level infection in a population. The dynamics of the host-parasite relationship during the inter-epizootic periods is poorly understood.
Temperature is an important factor in the persistence of infection in fish populations. When water temperature is low, the parasite grows and develops more slowly. The growth period of trophonts on fishes ranges from 1 week at 20°C to 20 days at 7°C (Nigrelli et al., 1976; Noe and Dickerson, 1995; Aihua and Buchmann, 2001). Growth occurs at temperatures as low as 2-5°C (Bauer, 1953; Aihua and Buchmann, 2001). McCallum (1982) found no density-dependent constraints on the establishment of I. multifiliis infections in naive hosts. There was, however, significant variation in the numbers of parasites found on each fish. These differences were attributed to such factors as the amount of mucus produced by individual fishes, nutritional status and stress. In a subsequent study, McCallum (1986) examined the role of host death on the reproductive potential of I. multifiliis in a population of susceptible fishes. He concluded that the low prevalence between epizootics was consistent with the idea that I. multifiliis and fish populations are regulated by parasite-induced host mortality. He developed a mathematical model that qualitatively reproduced the observed epizootic behaviour of an I. multifiliis infection.
ReferencesTop of page
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