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Treatment of trichodiniasis in eel Anguilla
/
anguilla reared in recirculation systems in
Denmark: alternatives to formaldehyde
Hans C.K. Madsen
a, Kurt Buchmann
b, Stig Mellergaard
a,)a
Danish Institute for Fisheries Research, Fish Diseases Laboratory, Stigboejlen 4, DK-1870 Frederiksberg C, Denmark
b
Royal Veterinary and Agricultural UniÕersity, Stigboejlen 4, DK-1870 Frederiksberg C, Denmark
Received 21 April 1999; received in revised form 10 December 1999; accepted 14 December 1999
Abstract
Ž .
Treatment of trichodiniasis in recirculation eel farms using formalin 37% has been found insufficient. We have screened 30 different chemical substances for efficacy against natural
Ž .
infections with trichodinids Trichodina jadranica on skin and gills of eels. The following
Ž . Ž .
substances showed high parasiticidal effect: acriflavin 25 ppm , bithionol 0.1 ppm , chloramine
Ž . w Ž . Ž . Ž .
T 50 ppm , Detarox AP 45 ppm , malachite green 1 ppm , raw garlic 200 ppm , potassium
Ž . w Ž .
permanganate 20 ppm and Virkon PF vet. 20 ppm . Preliminary screening revealed that the anthelmintic, bithionol, and the decomposable disinfectants Detarox AP and Virkon PFw vet. were potential therapeutics and these were tested on infected eel stocks in recirculation production units. The following treatments showed a high parasiticidal effect: bithionol at 0.1 ppm in a
wŽ .
recirculation system including the biofilters; Detarox AP 45 ppm in recirculation systems with
w
Ž
the biofilters temporarily isolated for 1 h and Virkon PF vet. 40 ppm; 25 ppm at start
.
supplemented with 15 ppm 1 h later in rearing tanks temporarily isolated from recirculation systems for 3 h.q2000 Elsevier Science B.V. All rights reserved.
Keywords: Recirculation aquaculture; Trichodiniasis; Eel; Treatment
1. Introduction
Ž .
In Denmark, European eels Anguilla anguilla have been produced in heated
Ž23–258C recirculation systems with biofilters during the last two decades. Infestations.
)Corresponding author.
Ž . Ž .
E-mail addresses: kurt.buchmann@vetmi.kvl.dk K. Buchmann , sme@dfu.min.dk S. Mellergaard .
0044-8486r00r$ - see front matterq2000 Elsevier Science B.V. All rights reserved.
Ž .
Ž .
with the trichodinid Trichodina jadranica Raabe, 1958 Ciliophora: Trichodinidae on
Ž
gills and skin of cultured eels have caused substantial financial losses Lyholt and
.
Buchmann, 1995; Lyholt et al., 1998 . Heavily infected eels become lethargic, secrete
Ž
excessive mucus and lose appetite resulting in inhibition of growth Amlacher, 1972; Bauer et al., 1973; Schaperclaus, 1979; Mellergaard and Dalsgaard, 1987; Sanmartin et
¨
.
al., 1991; Lom and Dykova, 1992; Buchmann and Bresciani, 1997 .
´
Ž
Previously, trichodiniasis was effectively controlled with formalin 50–120 ppm, one
.
to two treatments per week , but it now appears insufficient to control the infection. Little information about treatment of protozoan parasites under production conditions in aquaculture has been published. Also, relatively few agents are available. In addition to the lack of information some of the known efficacious potent antiprotozoan substances
Že.g., malachite green and acriflavin have been categorised as potentially carcinogenic..
In order to find a more efficacious trichodiniasis control agent and reduce the human health hazards of formalin exposure we screened 30 potential chemical agents for efficacy against T. jadranica and tested the most promising candidates in recirculation production units.
2. Materials and methods
2.1. Locations
Two different eel farms with a reputation of having frequent outbreaks of trichodinia-sis were selected for the experiments
2.2. Infection leÕel.
Ž . Ž .
Small pigmented eels elvers 1–30 g were examined by scraping mucus with a scalpel from the total surface of skin and of the four gill arches from one side of the eel.
Ž .
Larger eels 70–250 g were scraped only once on the central upper dorsal part of the body at the border to the dorsal fin in one third of the length of the eel. On eels of this
Ž . Ž
size the majority of trichodinids T. jadranica were found on the skin unpublished
.
data . Sampled mucus was transferred to glass slides and examined for trichodinids
Ž
microscopically. The approximate number of trichodinids number on skin and gills
.
pooled on small eels and on larger eels were converted to one out of five different infection categories for each fish: 0 parasitesscategory 0; 1–10 parasitesscategory 1; 11–100 parasitesscategory 2; 100–1000 parasitesscategory; 1000–10 000 parasites
Ž .
scategory 4. The infection level in a group nG10 of examined fish was expressed as the mean of the infection category of each fish. Mean infection categories were primarily used as an indicator of shifts in the infection levels within a stock of fish.
2.3. Aquarium trials
2.3.1. Screening substances
The chemicals selected for screening of efficacy against T. jadranica are listed in Table 1. Low pH and sodium chloride are included in ranges, which could be of interest for the farmers. Extreme nitrate concentrations were tested, too, because relative high
Ž y.
Ž .
according to the eel farmers. Infected pigmented eels mean weight, 4.5 g removed
Ž
from the production systems were introduced into plastic aquaria 20 l water originating from the rearing tanks, characteristics: 5–15 mg organic dry matterrl, pH range
.
6.5–7.0, temperature 25"18C . During the exposures ammonia was removed from the
Ž .
water using ‘‘biofilters’’ Power filter, 3 l, EHEIM 2213, Germany . Groups of 10 infected eels were exposed to the different chemicals in aquaria without any water exchange and the mean infection category was determined 24 h after the initial exposure. A substance was considered effective if all or almost all parasites were killed at a concentration not toxic to eels. In order to establish the therapeutic dose, replicate experiments were conducted with the effective substances in concentrations in the vicinity of the lowest dose needed for a good parasiticidal effect. Substances lethal to eels were considered ineffective.
2.3.1.1. Effects on eel. Substances were considered toxic if they caused nonreversible
Ž .
effects on eels e.g., spasms, loss of equilibrium, death and as nontoxic if only short-term reversible effects on eels were observed; e.g., slightly elevated mucus secretion was noted as a nontoxic effect.
Ž .
2.3.1.2. Effect of exposure time. Five eelsrgroup were exposed to bithionol 0.1 ppm or
w Ž .
Virkon PF vet. 20 ppm for 1, 2, 3 or 4 h and afterwards transferred to water without substance and examined for trichodinids during the fourth hour. Eels were exposed to
w Ž .
Detarox AP 45 ppm for 1 2, 1, 11 2 or 2 h and examined during the second hour. The shortest exposure times needed to remove all or almost all parasites were used as exposure time for the experimental treatments under farmed conditions. All
concentra-Ž .
tions reported are nominal concentrations. Bithionol was suspended in ethanol 1:20 ; control eels were exposed to an equal amount of solvent as used in the treated group.
2.3.2. Tolerance of eels to chemicals
Ž . w Ž .
The acute and chronic toxity of bithionol 0.05–1 ppm , Detarox AP 10–150 ppm
w Ž . Ž .
and Virkon PF vet. 10–100 ppm in pure tap water pHs7.2, 24"18C was
Ž . Ž .
examined in pigmented mean weight, 6.6 g and glass eels mean weight, 0.34 g . Because Virkon PFw
vet. may catalyse the conversion of chloride ions to gaseous
Ž
chlorine at relatively high salinities personal communication, Pharmacia and Upjohn,
. w
Copenhagen the toxicity of Virkon PF vet. to pigmented eels was determined in tap water modified to salinities of 5, 10 and 15 ppt. The various salinities were obtained by adding NaCl to tap water at 248C. Groups of seven eels were exposed to different concentrations of the substances for 5 and 96 h. The exposed groups were transferred to tap water after 5 h of exposure and monitored for an additional 91 h.
2.4. Full-scale trials in eel farms
w w Ž . Ž
Bithionol, Detarox AP and Virkon PF vet. as well as formalin 37% as a
.
Table 1
Parasiticidal effect of various chemicals on Trichodina jadranica in eel. Trials were conducted as 24 h water
Ž .
bath exposure 258C of infected eels. Infection levels are stated as infection categories posttreatment
w xŽ . Ž . w x Ž . w x Ž . w
Origin of substances product number other data : 1 Sigma A 8251 . 2 Sigma A 8126 . 3 Sigma T
x Ž . w x Ž . Ž
9881 . 4 BDH, UK 27670 4E . 5 Perdomini, Verona, Italy 15–25% peracetic acid, 4–5% hydrogen
. Ž . Ž . Ž . w x Ž . w x Ž .
peroxide . 6 : Raw and squeezed . 7 Merck 1.01398.0025 . 8 Fluka 60459 . 9 Antec International, UK
Ždecomposable inorganic salts, alcylbenzene-sulphonateŽ)90 % biogradability under OECD test conditions .. Ž10 Sigma A 0542 . 11 Sigma S 8259 . 12 Jansen Pharmaceutica, Beerse, Holland. 13 Fluka 25745 .. w x Ž . w x Ž . Ž . w x Ž14 Duphar, Wees, Holland diflubenzuron . 15 Sigma D 7044 . 16 Hoechst. 17 DAK 726604 . 18. Ž . Ž . w x Ž . Ž . w x Ž .
w xŽ . Ž . w x Ž . w x Ž . Ž
Riedel-de Haen, Germany 31440 sodium nitrate . 19 Sigma M 2004 . 20 Sigma O 0877 . 21¨ Ph. Eur.,
. Ž . Ž . Ž .
index 1272 . 22 Lowered with hydrochloric acid, eels came from pH 7.2 . 23 Pedersen J.L., Nibe,
Ž . w x Ž . Ž . Ž . Ž .
Denmark. 24 RBI, MA, USA Q-106 . 25 Raised from 3000 to 13,000 ppm . 26 Ph. Eur., index 1552 .
Ž27 pH. s7.2. 28 Orion. 29 Bayer. 30 Fluka 53260 .Ž . Ž . Ž . w x
Substances with parasiticidal Treatment Control, mean Treated, mean % Dead eels
Ž .
effect data on substance concentration infection category infection category in treated group
Žppm. ŽS.D.. ŽS.D.. due to toxicity
Ž . Ž . Ž .
Acriflavin hydrochlorid 1 25 2.2 0.6 0.0 0.0 0
Ž . Ž . Ž .
Acriflavin neutral 2 20 2.4 0.7 0.1 0.3 0
Ž . Ž .
Potassium permanganate 8 10 2.4 0.7 1.2 0.4 0
Ž . Ž .
Bithionol sulfoxide 11 0.25 2.3 0.5 2.1 0.3 0
wŽ . Ž . Ž .
Carnidazole 12 25 2.5 0.5 2.3 0.3 0
Ž . Ž . Ž .
Chloroquine diphosphate 13 100 2.0 0.0 1.3 0.7 0
wŽ . Ž . Ž .
Dimilin 14 50 2.5 0.5 1.7 0.6 0
Ž . Ž . Ž .
Halazone 15 10 2.5 0.5 2.6 0.5 50
Ž . Ž . Ž .
Hydrogen peroxide, 40% 1000 4 h 2.7 0.5 2.3 0.5 60
Ž . Ž . Ž .
Imidocarb dipropionate 16 30 2.6 0.5 1.3 0.5 0
Ž . Ž . Ž .
Ž .
Table 1 continued
Substances with parasiticidal Treatment Control, mean Treated, mean % Dead eels
Ž .
effect data on substance concentration infection category infection category in treated group
Žppm. ŽS.D.. ŽS.D.. due to toxicity
Ž . Ž . Ž .
Nitrate 18 3000 2.0 0.8 2.2 0.4 0
Ž . Ž . Ž .
N-methyl-glucamine 19 50 2.5 0.5 1.4 0.5 0
Ž . Ž . Ž .
Oxolinic acid 20 50 2.2 0.4 2.8 0.4 0
Ž . Ž . Ž .
Oxytetracycline 21 80 2.5 0.5 2.1 0.6 0
Ž . Ž . Ž .
pH 5 22 2.1 0.6 2.4 0.5 0
Ž . Ž . Ž .
Potassium oleat, 35% 23 4 2.0 0.8 2.0 0.0 60
Ž . Ž . Ž .
Quinidine sulphate 24 30 2.6 0.5 2.6 0.5 0
Ž . Ž . Ž .
Sodium chloride 25 4000 1.8 0.5 1.5 0.5 0
Ž . Ž .
10 000 2.8 0.4 2.6 0.5 0
Ž . Ž . Ž .
Sulfadimidinum 26 75 2.5 0.5 2.5 0.5 0
Ž . Ž . Ž .
Tap water 27 2.8 0.4 2.5 0.5 0
wŽ . Ž . Ž .
Tiguvon 28 20 2.8 0.4 3.0 0.0 20
Ž . Ž . Ž .
Toltrazuril 29 5 2.3 0.7 2.6 0.5 20
Ž . Ž . Ž .
4-Hexylresorcinol 30 1 2.3 0.6 1.3 0.6 70
a
In tap water.
Žincluding the biofilters Žbithionol and formalin , to the recirculation unit while..
Ž w .
biofilters were isolated temporarily 1 h, Detarox AP and formalin or to one or more
Ž w.
rearing tanks temporarily isolated from recirculation 3 h, Virkon PF . In the recircula-tion unit, the substances were added to the water reservoir supplying the rearing tanks. If biofilters were included during the experiment, treated fish were examined 3–4 h after the initial exposure. If biofilters were isolated during the experiment the treatment was regarded finished when rearing tanks were reconnected to biofilters and the fish were examined the following hour. For the bath treatments in separated tanks, untreated eels in the same system were used as controls. Groups of eels caught before treatment and transferred to the aquarium with system water were used as controls for treatments involving the entire recirculation system. Number and size of eels in a control group
Ž .
equalled the number of eels from the treated group Table 3 . Reinfection of treated eels
Ž
was examined 3 and 7 days after some of the treatments no control groups on days 3
. Ž
and 7 . Changes in feeding activity and mortality were evaluated subjectively based on
.
experience 3–4 weeks posttreatments. Effects of treatment on biofilters were examined
Ž w y1.
by determining the ammonia concentration Merck , resolution: 0.5 mg l every second day for 1 week posttreatment. High increase of ammonia was assumed to indicate a negative effect of treatment.
3. Results
3.1. Aquarium trials
3.1.1. Screening substances
Ž .
Thirty substances formalin and tap water trials not included were screened for
Ž . Ž . Ž
. w
Ž . Ž y1 .
ppm , Detarox AP 30 ppm, tap water fresh raw squeezed garlic 0.2 g l , 200 ppm ,
Ž . Ž . w
Ž
malachite green 1 ppm , potassium permanganate 20 ppm and Virkon PF vet. 20
. w Ž .
ppm removed all trichodinids from the eel. Detarox AP 20 ppm, tap water; 45 ppm ,
Ž . Ž .
Chloramine T 50 ppm and formalin 75 ppm, tap water removed almost all the parasites. Chloramine T and potassium permanganate were toxic to eels in therapeutic concentrations, while none of the other effective substances appeared to be acutely toxic at a therapeutic dose. The remaining substances or concentrations showed no or little
Ž .
effect on the parasites; however, some were toxic to the eels Table 1 . For further
Ž . w Ž . w Ž
examination bithionol 0.25 ppm , Detarox AP 45 ppm and Virkon PF vet. 20
.
ppm were selected and these showed a high parasiticidal effect after 1, 1 and 3 h
Ž .
respectively Fig. 1 in aquarium experiments.
3.1.2. Tolerance
Bithionol caused mortality to pigmented eels and to glass eels at drug concentrations
Ž .
higher than 0.4 or 0.1 ppm for 5 or 96 h, respectively Table 2 . Mortality was observed
Ž .
Fig. 1. Effect of exposure duration. Mean infection categories of eels ns5 infected with T. jadranica. Eels
Ž . wŽ . w
were exposed to bithionol a , Detarox AP b or Virkon PF vet. Infection categories were determined 4 h
Ž . Ž .
Table 2
Tolerances of eels to Bithionol, Detarox APw
and Virkon PFw
vet.: maximal concentration of the substances
Žppm were 100% of the eels survived.
Substance 5 h 96 h
Bithionol Glass eels 0.4 0.1
Pigmented eels 0.4 0.1
w
Detarox AP Glass eels 25 25
Pigmented eels 100 70
w
Virkon PF vet. Glass eels 10 10
a
Pigmented eels 70 30
b
Pigmented eels 40 10
a
At 0, 5 and 10 ppt sodium chloride.
b
At 15 ppt sodium chloride.
after approximately 2–3 h of exposure. Mortality of pigmented eels occurred when exposed to Detarox APw
at concentrations higher than 100 or 70 ppm in 5 or 96 h,
Ž .
respectively Table 2 . Mortality was observed after approximately 1 h of exposure.
w Ž . w
Glass eels tolerated maximally 25 ppm Detarox AP Table 2 . Virkon PF vet. in concentrations higher than 70 or 30 ppm for 5 or 96 h, respectively, caused mortality to pigmented eels at a salinity of 0–10 ppt . At a salinity of 15 ppt Virkon PFw
vet. caused mortality at concentrations higher than 40 or 10 ppm at an exposure time of 5 or 96 h,
Ž . w
respectively Table 2 . Mortality was observed after 3–4 h of exposure. Virkon PF
Ž .
vet. concentrations higher than 10 ppm 0 ppt salinity caused mortality to glass eels at
Ž .
exposure times of both 5 and 96 h Table 3 . Mortality was observed after approximately 2 h of exposure.
3.2. Full-scale trials in eel farms
Bithionol at 0.1 ppm reduced the mean infection categories of 1.2 and 2.3 to 0.1
ŽTrial B1 and B2, Table 3 . The mean infection category increased to 1.5 within 1 week.
Ž .
posttreatment B1 . No negative effects on eels or biofilters were observed. Detarox APw concentrations of 45 or 55 ppm reduced the mean infection categories of 1.5–2.7
Ž .
to 0.0–0.2 D1, D2, D3, Table 3 . Seven days posttreatment the infection categories
Ž .
increased to 1.4 and 0.6 D1 and D3, respectively . After start of exposure the swimming activity of the eels increased. Between 1 and 11 2 h later their activity appeared to be normal. A few hours after reconnection of the biofilters, feeding activity was low after which the activity returned to normal. No increase in mortality was observed. Virkon PFw
vet. was administered as a bath treatment of 3 h in temporarily
Ž . w
isolated rearing tanks V1 and V2, Table 3 . Initial exposures of 20 ppm of Virkon PF vet. effective under laboratory conditions, did not provide sufficient control under
Ž . w
practical farm conditions data not shown . In subsequent exposures, Virkon PF vet. added to an initial concentration of 25 ppm and supplemented with 15 ppm 1 h later reduced the mean infection category from 2.9 to 0.1; 3 days posttreatment the category
Ž .
had increased to 1.4 V1 . When supplemented with extra 20 instead of 15 ppm a mean
Ž .
()
Experimental treatments of trichodiniasis in recirculation plants: Design and efficacy expressed as reduction of infection category. Treated eels were examined 1 h
Ž .
posttreatment duration of treatment: hours of isolation of tanksrbiofilters ; experiments B1, B2 and F2: eels examined 3 h after treatment initiation
Ž .
Experimental design Mean infection category S.D.
Ž .
Treatment ppm No. of Mean Treated Treatment Treatment in Isolation of Control Treated Treated 3 Treated 7
Ž .
examined weights group: in isolated the recircu- biofilters h days later days later
Ž . Ž . Ž .
eels g total weight tank s h lation system
activity increased but appeared to be normal 1–2 h posttreatment. No negative effects on feeding activity and mortality were observed. When the treated tanks were reconnected to the recirculation system no negative effects were seen on the feeding or on the biofilters. A bath treatment of formalin at 75 ppm for 3 h reduced the mean infection
Ž .
category from 3.0 to 1.0 F1, Table 3 . Formalin also reduced the mean infection category from 2.6 to 1.2 when added to a concentration of 85 ppm in a recirculation
Ž .
system biofilters isolated 1 h . However, the mean infection category increased to 2.8
Ž . Ž .
three days posttreatment F2 . Formalin 60 ppm added to a complete recirculation unit
Žbiofilters included had no apparent effect on the parasites, fish nor biofilters F3 . All. Ž .
tested substances caused a slightly elevated mucus secretion on skin and gills.
4. Discussion
4.1. Aquarium trials
Thirty different substances were screened as potential parasiticides for ectoparasitic T. jadranica in eels. Eight substances had a high parasiticidal effect and out of these the anthelmintic bithionol and the disinfectants, Detarox APw
and Virkon PFw
vet., appeared to be the best potential alternatives to formalin for treatment of trichodiniasis.
4.2. Full-scale trials in eel farms
Highly infected eels in production units were treated with bithionol, Detarox APw
and Virkon PFw
vet. Using these substances high infection levels in stocks with thousands of eels were reduced to levels where hardly any parasites were found. The outlined procedures caused a temporary elevated swimming activity and mucus secretion during treatment. The treatments caused no observable effects on the biofilters and the feeding activity was only reduced for a few hours.
Bithionol seemed to be attractive as a therapeutic because of its effectiveness and its ability to treat the entire recirculation system, although the drug has some serious disadvantages. Its therapeutic index was relatively narrow, so a minor overdosing might be toxic. In addition, intensive data must be developed describing bithionol residues and metabolites in eel flesh before introduction of this drug to aquaculture. Such work will probably not be implemented as long as it is possible to control trichodiniasis with easily decomposable oxidizing disinfectants. The quick acting Detarox APw is the most attractive substance as it can be added to the recirculation system with the biofilters isolated for only 1 h. Virkon PFw vet. required a treatment period of 3 h in isolated tanks and was considered to be an alternative to Detarox APw only.
None of the experimental treatments were capable of eradicating T. jadranica from production units. Although T. jadranica was undetectable after treatment with Detarox
w Ž .
AP 55 ppm trichodinids became apparent in few days, possible due to the
experimen-Ž w w .
tal procedures Detarox AP and Virkon PF vet. that did not remove trichodinids from the biofilters. A possible source of infection might be infected eels living in the biofilter and connecting pipe systems. Even if there were no parasites in the biofilters reinfection may still occur because one or more parasites survived the treatments, e.g.,
Ž .
trichodinids may be found deep in the epithelia Frank, 1962 . Treating trichodiniasis with current therapeutics should focus on controlling the abundance of the parasite, not on eradication. The interval between required treatments may depend on both the condition of fish and water quality. Weakened eels are more susceptible to infection
ŽLom and Dykova, 1992 and high organic load favours trichodinids Schaperclaus,
´
. Ž¨
.
1979; Stoskopf, 1993; unpublished data .
5. Conclusions
w
Ž .
Detarox AP 45 ppm appeared to be a proper alternative to formalin for treatment of trichodiniasis. Biofilters should be isolated for 1 h to minimise adverse effects. Detarox APw can be added to the water reservoir supplying the rearing tanks or if
w Ž .
isolation of biofilters is not possible, Detarox AP 45 ppm can be used for bath treatments in tanks isolated from the recirculation system for 1 h. Detarox APw
is a quick-acting oxidative agent and, therefore, dose levels higher than recommended must be avoided. Glass eels introduced to tap water might be treated with F20 ppm of Detarox APw
with care. Virkon PFw
vet. may be used as an alternative to Detarox APw
and should be administered as a 3-h bath treatment in isolated rearing tanks. Initial Virkon PFw
vet. concentration should be 25 ppm supplemented with 15 ppm 1 h later. Virkon PFw
vet. is not recommended for treatment of glass eels or any eels if salinity is higher than 10 ppt.
Acknowledgements
We are indebted to the owners and staff of Steensgaard Eel Farm, Randboel and Dyrkjaerslund Eel Farm, Baelum in Denmark for assistance during experiments. The project was funded by the Danish Directorate for Development of Aquaculture and Fisheries and Elisabeth and Knud Petersens Foundation.
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