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Diphyllobothrium Latum (Cestoda: Diphyllobothriidea) in Perch (Perca Fluviatilis) in Three Sub-Alpine Lakes: Influence of Biotic and Abiotic Factors on Prevalence

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Diphyllobothrium Latum (Cestoda: Diphyllobothriidea) in Perch (Perca Fluviatilis) in Three Sub-Alpine Lakes: Influence of Biotic and Abiotic Factors on Prevalence J. Limnol., 68(2): 167-173, 2009 DOI: 10.3274/JL09-68-2-01 Diphyllobothrium latum (Cestoda: Diphyllobothriidea) in perch (Perca fluviatilis) in three sub-alpine lakes: influence of biotic and abiotic factors on prevalence Barbara WICHT1,2)*, Costanzo LIMONI3), Raffaele PEDUZZI2) and Orlando PETRINI1) 1)Istituto Cantonale di Microbiologia, Bellinzona, Switzerland 2)Faculté des Sciences, Département de Botanique et Biologie Végétale, Laboratoire d'Ecologie Microbienne, Université de Genève, Geneva, Switzerland 3)Alpha5, Biometrics & Data Management, Riva San Vitale, Switzerland *e-mail corresponding author: [email protected] ABSTRACT In recent years, human diphyllobothriosis has staged a comeback in Swiss, French and Italian sub-alpine regions. The main putative infective source of the causative agent (the tapeworm Diphyllobothrium latum) in these areas is perch (Perca fluviatilis). Therefore, the occurrence of D. latum in this fish species was investigated between 2005 and 2008 in the sub-alpine lakes Maggiore, Lugano and Geneva. Prevalence in fish of Lake Maggiore was 14% (n = 880). In Lake Geneva, 5.1% fillets (n = 532) were infected, whereas perch from Lake Lugano were free from the parasite. These results are discussed in relation to previous studies. Data on fish size and weight indicate that infection of perch by D. latum is independent of age and sex. Abiotic factors considered critical for D. latum life cycle (water temperature and oxygen concentration) characterize the three basins and were related to their infestation frequencies. The presence of this parasite was most likely favoured by warmer, well oxygenated waters. Previous studies indicate that the lake’s trophic state (i.e. content of total phosphorus) influenced the availability of the first intermediate hosts (copepods) of some pseudophyllideans. In our study, no correlation was observed between the amount of phosphorus and the number of copepods in populations of zooplankton. Nevertheless, the trophic states of the three lakes seemed to affect the degree of infection in fish. In conclusion, at least in sub-alpine lakes, abiotic factors such as water temperature, oxygenation and trophic state seem to have an influence on maintaining or preventing perch infection with D. latum. Key words: food-borne zoonoses, emerging infections, flatworms, helminths al. 2005); 7.8% in Lake Maggiore and 30% on average 1. INTRODUCTION in Lake Como (Bonini et al. 1998; Gustinelli et al. Human diphyllobothriosis is a cosmopolitan fish- 2007). However, some basins located in this region, borne zoonosis caused by tapeworms of the genus such as lakes Varese and Lugano, were free from the Diphyllobothrium (Cestoda: Diphyllobothriidea). The parasite (Dupouy-Camet & Peduzzi 2004). life cycle of the causative agent includes two intermedi- The presence of definitive hosts releasing eggs in ate hosts (copepods and fish) and a definitive host (a water is obviously among the major requirements for fish-eating mammal, mainly man). In the last 20 years, maintaining Diphyllobothrium in a water system. This this disease has experienced an unexpected comeback in condition being satisfied in endemic sub-alpine areas, Swiss, French and Italian sub-alpine regions (Dupouy- environmental factors might play a role in the develop- Camet & Peduzzi 2004; Peduzzi 1990). Epidemiologi- ment of ontogenetic stages of this tapeworm. Abiotic cal monitoring and molecular identification of clinical parameters such as water temperature, oxygen concen- cases in this area have revealed the presence of D. latum tration (because eggs are aerobic) and light affect (the main autochthonous species infecting humans), as Diphyllobothrium embryonic development and the well as D. nihonkaiense and D. dendriticum (alloch- hatching of eggs (von Bonsdorff 1977). Moreover, for tonous species; Yéra et al. 2006; Wicht et al. 2007; some freshwater fish parasites that depend on zoo- Wicht et al. 2008; Paugam et al., in press). Perch (Perca plankton for their development, the availability of these fluviatilis) was identified as a frequent host of plerocer- hosts has been linked to the lake’s trophic state (deter- coid larvae of D. latum. In the past years, a high preva- mined by total phosphorus). Thus, oligotrophic condi- lence in this fish has been demonstrated in several sub- tions may lead to an increased ratio of copepods to alpine lakes: up to 33% of the population investigated cladocerans (Molzen 2005). On the contrary, eutrophic was infected in Lake Orta (Northern Italy; Peduzzi & conditions would increase the proportion of cladocerans Boucher-Rodoni 2001); from 3.7% to 14.2% in the in zooplankton, reducing the availability of copepods as lakes of Bienne and Morat (Swiss Plateau; Golay & first intermediate hosts and therefore impairing the Mariaux 1995); 4-10% in Lake Geneva (Nicoulaud et parasitic life cycle. The trophic state could therefore 168 B. Wicht et al. represent another crucial component for the mainte- ermen. Size (total length, measured from the extremity nance of Diphyllobothrium in a water body. To our of the head until the inferior lobe of the tail) and sex knowledge, no previous studies that include these vari- were recorded for each fish. Both whole individuals and ables have been conducted on the occurrence of fillets were weighted. Diphyllobothrium in sub-alpine lakes. Plerocercoids were isolated by visual inspection and The main objective of this study was to survey the successively identified by molecular methods. DNA occurrence of diphyllobothriosis in perch of the lakes was extracted from each larva following the Tissue Maggiore, Lugano and Geneva from 2005 to 2008. Fish Protocol of the QIAamp DNA Minikit (QIAGEN, samples were checked for the presence or absence of Hombrechtikon, Switzerland). About 50 ng µL-1 DNA plerocercoid larvae, the identity of which was confirmed were tested by polymerase chain reaction using the Taq with molecular methods. Biotic (weight, size and sex of PCR Master Mix Kit (QIAGEN, Hombrechtikon, Swit- the fish) and abiotic factors affecting embryonation and zerland), with specific primers for cytochrome c oxidase egg hatching (water temperature and dissolved oxygen), subunit I (Cox-1) complete gene amplification (Nakao were also taken into account. Trophic states of these et al. 2007). This mitochondrial gene is considered as lakes, evaluated by rates of total phosphorus in the the most discriminant within Diphyllobothrium (Isobe et epilimnion, were correlated with the occurrence of the al. 1998; Yéra et al. 2008). Amplicons were directly parasite and the presence of its first intermediate hosts. purified with NucleoSpin® Extract II Kit (Macherey- Nagel, Oensingen) and DNA was quantified with a ND- 2. METHODS 100 Spectrophotometer (NanoDrop Technologies Inc., 2.1. Sampling Wilmington, USA). Sequencing reaction was prepared using the ABI PRISM® BigDyeTM Terminator v1.1 The study was carried out from July 2005 to June Cycle Sequencing Kit (Applied Biosystems, Rotkreuz, 2008. Samples of perch (Perca fluviatilis) were col- Switzerland). After purification by filtration through lected usually once in each season. MF™ membrane filters 0.025 µm (Millipore, Zug, In Lake Maggiore, at least 200 individuals were Switzerland), samples were loaded in an automatic collected each year. Fish were caught using gill nets sequencer (ABI PRISM® 310 Genetic Analyzer, Perkin with 28 × 28 mm mesh. Due to unfavorable weather Elmer, Rodgau-Jügesheim, Switzerland). Manually cor- conditions, sampling in winter 2007 could not be per- rected sequences were aligned in a Neighbor-Joining formed. Fifteen stations [Brissago, Porto Ronco, tree (Kimura-2 parameters; bootstrap values for 1,000 Ascona, Locarno, Muralto, Tenero, Foce Verzasca, replicates; MEGA version 3.0; Kumar et al. 2004) and Magadino, Vira Gambarogno, San Nazzaro, Gerra analysed by a BLAST search (Altschul et al. 1990). Gambarogno and Ranzo (Swiss part), Cannero, Baveno and Monvalle (Italian part)] were chosen to obtain a 2.3. Statistical analyses representative sample for the whole lake. In Lake Geneva, a regular monitoring was carried The prevalence of Diphyllobothrium in the samples was calculated for each lake. The age of the fishes was out only from June 2006 to January 2008, as previous data were taken from Nicoulaud et al. (2005). Samples estimated from their weight and size according to Negri consisted mainly of perch fillets provided by local fish- (2000) and Muus et al. (1971). Missing weights of either fish or fillets were esti- ermen. Six stations were chosen in Petit Lac (Mies and Versoix, Canton Geneva, Switzerland) and in Grand mated using the formula: Lac (Morges and Paudex in Canton Vaud, Switzerland; Fillet weight = 1.915 + 0.213 × Fish weight (1 Séchex and Thonon-les-Bains in department of Haute- derived from a regression analysis performed on the Savoie, France), which are characterized by different samples for which both fillets and whole fish weights depths and intervals of water mixing, leading to differ- were available (r2 = 0.95). ent concentrations of oxygen and phosphorus The correlation between prevalence of infection and (Lazzarotto et al. 2006). estimated weight, size, and sex of fish were checked Lake Lugano was sampled once in October 2005 graphically and using a chi square test. Perch show dif- and once in January 2006, and seasonally thereafter ferent linear and weight growth curves depending on using gill nets with 32 × 32 mm mesh. Eight stations their sex (Negri 2000). Correlation between fish weight
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